Plant Innate Immunity Signals and Signaling Systems: Bioengineering and Molecular Manipulation for Crop Disease Management (Signaling and Communication in Plants) 940241939X, 9789402419399

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Signaling and Communication in Plants

P. Vidhyasekaran

Plant Innate Immunity Signals and Signaling Systems Bioengineering and Molecular Manipulation for Crop Disease Management

Signaling and Communication in Plants Series Editor František Baluška, IZMB, Department of Plant Cell Biology, University of Bonn, Bonn, Nordrhein-Westfalen, Germany

More information about this series at http://www.springer.com/series/8094

P. Vidhyasekaran

Plant Innate Immunity Signals and Signaling Systems Bioengineering and Molecular Manipulation for Crop Disease Management

123

P. Vidhyasekaran Department of Plant Pathology Tamil Nadu Agricultural University Coimbatore, Tamil Nadu, India

ISSN 1867-9048 ISSN 1867-9056 (electronic) Signaling and Communication in Plants ISBN 978-94-024-1939-9 ISBN 978-94-024-1940-5 (eBook) https://doi.org/10.1007/978-94-024-1940-5 © Springer Nature B.V. 2020 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature B.V. The registered company address is: Van Godewijckstraat 30, 3311 GX Dordrecht, The Netherlands

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1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 Signals and Signaling Systems Involved in Activation of Plant Innate Immune System . . . . . . . . . . . . . . . . . . . . . 1.2 Bioengineering Technologies to Activate Plant Immunity Signaling Systems for Management of Crop Diseases . . . . . 1.3 Molecular Manipulation of Plant Immunity Signaling Systems Using Abiotic or Biotic Elicitors for Management of Crop Diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Manipulation of Calcium Ion Influx—Mediated Immune Signaling Systems for Crop Disease Management . . . . . . . . . . 2.1 Ca2+ Signaling Components . . . . . . . . . . . . . . . . . . . . . . 2.2 Bioengineering G-Proteins for Plant Disease Management . 2.3 Engineering Glutamate-Gated Ca2+ Channel for Plant Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Engineering H+-ATPase for Plant Disease Management . . 2.5 Molecular Manipulation of H+-ATPase Proton Pump by Laminarin for Crop Disease Management . . . . . . . . . . 2.6 Manipulation of H+-ATPase Using Chitosan Commercial Formulations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.7 Engineering Annexins for Crop Disease Management . . . . 2.8 Bioengineering Calmodulin Genes to Promote Immune Responses for Plant Disease Management . . . . . . . . . . . . 2.9 Engineering CBP60g Calmodulin-Binding Proteins for Disease Management . . . . . . . . . . . . . . . . . . . . . . . . .

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2.10 Engineering Calcium-Dependent Protein Kinase Genes for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . 2.11 Manipulation of Ca2+-Dependent Signaling Pathway by Vitamin B1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Manipulation of Reactive Oxygen Species, Redox and Nitric Oxide Signaling Systems to Activate Plant Innate Immunity for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Complexity of ROS-Redox-NO Signaling System . . . . . . . . . 3.2 Manipulation of ROS Signaling System Using Benzothiadiazole (BTH) for Crop Disease Management . . . . . . . . . . . . . . . . . . 3.2.1 BTH Triggers Oxidative Burst and Accumulation of ROS Through Phospholipid Signaling . . . . . . . . . . 3.2.2 BTH Triggers Accumulation of ROS Through Action of Peroxidases and Superoxide Dismutases . . . 3.2.3 BTH May Trigger Accumulation of ROS Through Suppression of ROS-Degrading Enzymes . . . . . . . . . 3.2.4 Fine-Tuning of Accumulation of ROS by BTH . . . . . 3.2.5 BTH Activates NPR1 by Inducing ROS-Mediated Redox Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.6 BTH Primes the Plants for Faster and Stronger Production of ROS . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.7 Manipulation of Peroxidases by BTH for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.8 BTH Induces Several Host Plant Defense Responses Downstream of ROS Signaling . . . . . . . . . . . . . . . . . 3.2.9 Management of Fungal Diseases in Crop Plants by Triggering Immune Responses Using BTH . . . . . . 3.2.10 Management of Oomycete Diseases of Crop Plants by Triggering Plant Immune Responses Using BTH . . 3.2.11 Management of Bacterial Diseases in Crop Plants by Triggering Plant Immune Responses Using BTH . . 3.2.12 Management of Virus Diseases in Crop Plants by Triggering Plant Immune Responses Using BTH . . . . 3.2.13 Management of Phytoplasma Diseases of Crop Plants by Triggering Plant Immune Responses Using BTH . . 3.2.14 Management of Parasitic Plants by Manipulation of ROS Signaling System Using BTH . . . . . . . . . . . . 3.3 Manipulation of ROS and Redox Signaling Systems Using Riboflavin to Promote Plant Immunity Potential for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Molecular Manipulation of ROS-Mediated Redox Signaling System Using Menadione Sodium Bisulphite for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Management of Crop Diseases Using Thiamine Through Manipulation of ROS Signaling System . . . . . . . . . . . . . . . . . 3.6 Manipulation of ROS and Redox Signaling Systems Using Herbicides to Activate Plant Immune Signaling System for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . 3.6.1 Management of Crop Diseases Using Lactofen Through Singlet Oxygen-Mediated ROS Signaling System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6.2 Management of Crop Diseases Using Trifluralin Through Manipulation of ROS-Mediated Redox Signaling System . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6.3 Management of Crop Diseases Using Glufosinate Ammonium Through Manipulation of ROS-Signaling System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7 Management of Crop Diseases Using Giant Knotweed Extract Through Activation of ROS Signaling System . . . . . . 3.8 Manipulation of ROS Signaling System Using b-Aminobutyric Acid for Crop Disease Management . . . . . . . . . . . . . . . . . . . 3.8.1 BABA Triggers ROS Production and Activates Plant Immune Responses . . . . . . . . . . . . . . . . . . . . . 3.8.2 BABA Primes NADPH Oxidase-Dependent ROS Production and Induces Disease Resistance . . . . . . . . 3.8.3 ROS Homeostasis May Regulate Primed Immune Responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.9 Manipulation of ROS Signaling System Using Phosphorous Compounds for Crop Disease Management . . . . . . . . . . . . . . 3.9.1 Potassium Phosphonate Triggers ROS Signaling System-Mediated Plant Defense Responses . . . . . . . . 3.9.2 K2HPO4 Triggers ROS Signaling in Plant Immune System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.10 Reactive Oxygen Species Generators as Plant Innate Immunity System Activators for Crop Disease Management . . 3.11 Manipulation of ROS and Redox Signaling System Using Microbes to Trigger Immune Responses for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.11.1 Pseudomonas aeruginosa Induces ISR by Triggering ROS Signaling System . . . . . . . . . . . . . . . . . . . . . . . 3.11.2 Pseudomonas fluorescens WCS374r Induces ROS-Mediated Disease Resistance . . . . . . . . . . . . . . 3.11.3 Serratia plymuthica Primes Plants for Enhanced Attacker-Induced Accumulation of ROS and Triggers ISR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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3.11.4 Bacillus mycoides Elicits Systemic Induced Resistance by Triggering ROS Production . . . . . . . . . . . . . . . . . 3.11.5 Bacillus pumilus Triggers ROS-Mediated Induced Systemic Resistance . . . . . . . . . . . . . . . . . . . . . . . . . 3.12 Manipulation of ROS Signaling by Silicon to Activate Plant Innate Immune Responses . . . . . . . . . . . . . . . . . . . . . . 3.13 Bioengineering Cysteine-Rich Receptor-Like Kinase (CRK) Genes to Activate ROS-Modulated Plant Immune Responses for Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.14 Bioengineering Lectin Receptor Kinase (LecRK) Genes to Activate ROS-Modulated Plant Immune Responses for Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.15 Engineering Peroxidase Gene to Activate ROS-Mediated Plant Immune Responses for Crop Disease Management . . . . . 3.16 Bioengineering Superoxide Dismutase to Activate ROS-Mediated Immune Signaling for Disease Management . . 3.17 Engineering Glucose Oxidase Gene to Trigger ROS Production for Management of Crop Diseases . . . . . . . . . . . . 3.18 Manipulation of NO Signaling System to Activate Plant Immune Responses for Disease Management . . . . . . . . . . . . . 3.18.1 Manipulation of S-Nitroso Glutathione Reductase (GSNOR) for Plant Disease Management . . . . . . . . . 3.18.2 Engineering Mammalian Nitric Oxide Synthase Gene for Crop Disease Management . . . . . . . . . . . . . 3.18.3 Manipulation of NO Signaling by Sodium Nitroprusside for Crop Disease Management . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Bioengineering and Molecular Manipulation of Mitogen-Activated Kinases to Activate Plant Innate Immunity for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 MAPK Signal Transduction System in Plant Innate Immunity . 4.2 Engineering Mitogen-Activated Protein Kinase (MAPK) Genes to Enhance Plant Immune Responses by Triggering Phosphorylation of Transcription Factors . . . . . . . . . . . . . . . . 4.3 Engineering Mitogen-Activated Kinase Kinase (MAPKK) Genes to Activate ROS Signaling System for Management of Crop Diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Engineering MAPK/MAPKK Genes to Activate Salicylate Signaling System for Management of Diseases . . . . . . . . . . . .

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Engineering MAPK Genes for Management of Pathogens by Activating JA Signaling System . . . . . . . . . . . . . . . . . . . 4.5.1 MPK4 Genes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5.2 MK1 Gene from Capsicum Annuum . . . . . . . . . . . . 4.6 Engineering MAPK Genes to Activate Salicylate-JasmonateEthylene Signaling Network for Crop Disease Management . 4.6.1 MAPKs Activate Plant Hormone Signaling Network 4.6.2 Cotton GhMPK16 Gene . . . . . . . . . . . . . . . . . . . . . 4.6.3 Cotton GhMPK2 Gene . . . . . . . . . . . . . . . . . . . . . . 4.7 Molecular Manipulation of MAPK Genes Which Negatively Regulate SA Signaling System for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.7.1 Manipulation of Arabidopsis MPK4 Gene . . . . . . . . 4.7.2 Manipulation of GmMPK4 . . . . . . . . . . . . . . . . . . . 4.7.3 Manipulation of OsMPK6 Gene . . . . . . . . . . . . . . . 4.8 Molecular Manipulation of SIPK-WIPK Genes Expression for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . 4.9 Molecular Manipulation of EDR1, a MAPKK Kinase for Plant Disease Management . . . . . . . . . . . . . . . . . . . . . . . 4.10 Manipulation of TIPK Gene Using Trichoderma for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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5 Bioengineering and Molecular Manipulation of Salicylic Acid Signaling System to Activate Plant Immune Responses for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1 Salicylic Acid Signaling System Activates Local Resistance, Systemic Acquired Resistance, and Transgenerational Systemic Disease Resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Bioengineering Genes to Trigger SA Biosynthesis and Accumulation for Crop Disease Management . . . . . . . . . . 5.2.1 Bioengineering Genes Encoding Enzymes Involved in SA Biosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.2 Engineering SA Signaling Regulator Protein Genes Involved in SA Production for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.3 Engineering RNA-Binding Protein Gene to Activate SA Biosynthesis Pathway . . . . . . . . . . . . . . . . . . . . . 5.2.4 Engineering Calmodulin-Binding Protein Gene to Trigger SA Biosynthesis for Disease Management . . . 5.2.5 Engineering WRKY Transcription Factor Genes to Activate SA Biosynthesis Genes for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Engineering Gene Encoding WIPK-Activated Transcription Factor to Increase Accumulation of SA for Crop Disease Management . . . . . . . . . . . 5.2.7 Engineering Ubiquitin-Proteasome Pathway Genes to Trigger SA Accumulation for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . 5.3 Bioengineering NPR1 Genes for Crop Disease Management . 5.3.1 NPR1 Is a Key Component in SA-Triggered SAR . . 5.3.2 Engineering Arabidopsis NPR1 Gene in Crop Plants for Disease Management . . . . . . . . . . . . . . . . . . . . . 5.3.3 Engineering NPR1-like Genes for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4 Manipulation of NPR1 Gene Expression by Synthetic Chemicals to Trigger Systemic Acquired Resistance (SAR) . . 5.4.1 Benzothiadiazole (BTH) Induces SA-Dependent SAR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4.2 N-Cyanomethyl-2-Chloroisonicotinamide (NCI) Activates NPR1-Dependent Defense Responses . . . . 5.4.3 Tiadinil (TDL) Activates NPR1 Gene to Induce SAR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4.4 SV-03 Activates NPR1 Gene to Induce SAR . . . . . . 5.5 Molecular Manipulation of SA Signaling System by Probenazole for Crop Disease Management . . . . . . . . . . . . . 5.6 Induction of Transgenerational SAR by BABA . . . . . . . . . . 5.7 Manipulation of SA Signaling System Using Plant-Derived Products for Disease Management . . . . . . . . . . . . . . . . . . . . 5.7.1 Azelaic Acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.7.2 AHO, a Product from Strobilanthes . . . . . . . . . . . . . 5.7.3 Burdock Plant Oligosaccharide Product . . . . . . . . . . 5.8 N-Acyl-L-Homoserine Lactones (AHLs)–Producing Bacteria Induce SA-Dependent Systemic Resistance . . . . . . . . . . . . . 5.9 Activation of SA-Dependent Signaling System by Rhizobacteria for Management of Crop Diseases . . . . . . . . . 5.10 Manipulation of SA Signaling System Using Yeast Elicitor for Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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6 Bioengineering and Molecular Manipulation of Jasmonate Signaling System to Activate Plant Immune System for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223 6.1 Jasmonate Signaling System Triggers Local and Induced Systemic Resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224 6.2 Bioengineering Genes Encoding Enzymes in JA Biosynthesis Pathway . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225

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Enzymes Involved in JA Biosynthesis Pathway . . . . . Engineering Lipoxygenase Genes to Develop DiseaseResistant Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2.3 Engineering Allene Oxide Synthase Gene to Trigger JA Production for Crop Disease Management . . . . . . 6.3 Manipulation of Genes Encoding Enzymes Involved in JA Biosynthesis Using Alkamide . . . . . . . . . . . . . . . . . . . . . . . . 6.4 Molecular Manipulation of Lipoxygenase Enzyme Involved in JA Biosynthesis by Chitosan for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.5 Bioengineering for Production of Arachidonic Acid in Plants to Activate JA Biosynthesis Pathway Genes for Disease Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.6 Manipulaion of JA-Dependent Signaling System Using Hexanoic Acid for Plant Disease Management . . . . . . . . . . . . 6.7 Manipulation of Jasmonic Acid Signaling Pathway Using Ulvan for Crop Disease Management . . . . . . . . . . . . . . . . . . . 6.8 Engineering Transcription Factor Genes to Manipulate JA Signaling System for Crop Disease Management . . . . . . . . . . 6.9 Manipulation of JA Signaling System Using Microbes for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . 6.9.1 Trichoderma asperellum . . . . . . . . . . . . . . . . . . . . . . 6.9.2 Trichoderma virens . . . . . . . . . . . . . . . . . . . . . . . . . 6.9.3 Trichoderma harzianum . . . . . . . . . . . . . . . . . . . . . . 6.9.4 Pseudomonas putida BTP1 . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Bioengineering and Molecular Manipulation of Ethylene Signaling System for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . 7.1 Ethylene Signaling System Triggers Local and Induced Systemic Resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2 Molecular Manipulation of Ethylene Biosynthesis Pathway for Crop Disease Management . . . . . . . . . . . . . . . . . . . . . . . . 7.3 Engineering ERF Genes to Manipulate Ethylene Signaling System for Crop Disease Management . . . . . . . . . . . . . . . . . . 7.4 Bioengineering EIN2 Gene to Activate Ethylene Signaling System for Crop Disease Management . . . . . . . . . . . . . . . . . . 7.5 Molecular Manipulation of Ethylene-Dependent Signaling System Using Microbes for Crop Disease Management . . . . . 7.5.1 Rhizobacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5.2 Trichoderma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5.3 Pythium oligandrum . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Chapter 1

Introduction

Abstract Several signals and signaling systems are involved in activation of plant immune system. Early and robust activation of plant immunity signaling systems triggers strong defense responses against pathogens. Enhancing disease resistance through altered regulation of these signaling systems has been shown to be an attractive technology for management of crop diseases. This book describes various bioengineering and molecular manipulation techniques to activate calcium ion influx–mediated immune signaling system, reactive oxygen species signaling system, nitric oxide signaling system, MAPK signal transduction system, salicylate (SA) signaling system, jasmonate (JA) signaling system, and ethylene signaling system. Ca2+ signaling system involves voltage-dependent Ca2+ -permeable ion channels, cyclic nucleotide-gated channels, glutamate receptor-like ion channels, calcium transporters, calcium ion pumps, carriers, and Ca2+ efflux channels, Bioengineering gene encoding glutamate receptor-like ion channel protein has been found to be a useful technology to develop disease resistant plants. The transgenic plants expressing the H+ -ATPase proton pump show enhanced resistance against viral, bacterial, and oomycete pathogens. Annexin is a Ca2+ -permeable transporter. The transgenic tobacco plants expressing the annexin gene show enhanced disease resistance. Calcium-dependent protein kinases (CDPKs) are Ca2+ sensor proteins in transducing differential Ca2+ signatures activating complex downstream responses. Transgenic plants overexpressing calcium-dependent protein kinase gene show enhanced disease resistance. Several G-protein genes have been cloned and used for engineering to develop transgenic plants expressing enhanced resistance against bacterial, fungal, and viral diseases. Cysteine-rich receptor-like kinases (CRKs) are connected to redox and ROS signaling. Transgenic plants overexpressing CRK genes show enhanced disease resistance by triggering enhanced ROS production. L-type lectin receptor kinases (LecRKs) have been exploited to develop transgenic diseaseresistant plants. These transgenic plants show enhanced production of ROS and trigger defense responses against pathogens. Peroxidases in the cell wall can generate apoplastic H2 O2 and transgenic plants overexpressing peroxidase gene show

© Springer Nature B.V. 2020 P. Vidhyasekaran, Plant Innate Immunity Signals and Signaling Systems, Signaling and Communication in Plants, https://doi.org/10.1007/978-94-024-1940-5_1

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enhanced disease resistance. Super oxide dismutase gene has been engineered to activate ROS-mediated immune signaling for disease management. Fungal glucose oxidase gene has been engineered to develop disease-resistant plants. Expression of the fungal glucose oxidase gene leads to elevated production of H2 O2 in the transgenic plants resulting in increased disease resistance. Nitric oxide (NO) signaling system can also be manipulated for disease management. GSNOR (S- nitroso glutathione reductase) has been exploited using antisense strategy to develop transgenic plants expressing resistance against oomycete and bacterial pathogens. Mitogenactivated protein kinases (MAPKs) are important components in the plant immune signal transduction system and they transduce extracellular stimuli into intracellular transcription factors. Technologies have been developed to utilize appropriate MAPK genes for developing disease-resistant plants. Plants do not have much endogenous SA and by increasing the SA content, defense genes can be activated. The endogenous SA level can be increased by engineering ICS, IPL, PAD4, AtRBP-DR1, OsWRKY13, OsWRKY89, and SGT1 genes and the transgenic plants overexpressing these genes show enhanced accumulation of SA and disease resistance. NPR1 gene is a master regulator of the SA-mediated induction of systemic acquired resistance (SAR). NPR1 gene has been exploited to develop disease-resistant transgenic plants. Genes encoding phospholipases, lipoxygenases (LOXs), allene oxide synthase (AOS), allene oxide cyclase (AOC), and OPDA reductase (OPR) have been cloned and engineered to enhance jasmonate (JA) biosynthesis and JA accumulation activates plant immune system. Arachidonic acid isolated from microbes is an elicitor of plant defense responses. Bioengineering technology has been developed to make the plants themselves to produce arachidonic acid. The arachidonic acid-containing transgenic plants show increased levels of jasmonic acid. Developing transgenic plants constitutively producing arachidonic acid may be a potential approach to activate JA pathway for management of plant diseases. Some transcription factor genes have been engineered to manipulate JA signaling system for crop disease management. Under natural conditions endogenous ethylene content is very low in plants and its level is not sufficient to induce defense gene expression. Increase in ethylene biosynthesis induces enhanced defense responses. Transgenic rice lines overexpressing ACC synthase gene, OsACS2, have been generated and these transgenic plants show increased levels of endogenous ethylene and disease resistance. Several biotic and abiotic elicitors have been successfully utilized to activate the plant immune system for management of crop diseases. Laminarin manipulates the proton pump and triggers defense responses. Chitosan treatment inactivates H+ -ATPase resulting in membrane depolarization, which is involved in increasing Ca2+ influx. Chitosan has been found to be highly effective in inducing resistance against oomycete, fungal, viral, and bacterial diseases. Thiamine treatment triggers Ca2+ influx and induces Ca2+ -induced protein kinase C (PKC) activity. It effectively controls bacterial, fungal, and viral diseases of crop plants by activating Ca2+ signaling system. BTH (benzo[1,2,3]thiadiazole-7-carbothioc acid S-methyl ester) is the most successfully developed commercial compound to manipulate ROS signaling system for management of viral, bacterial, and phytoplasma diseases and parasitic plants. Riboflavin is another compound which can be used to manipulate ROS and redox signaling system.

1 Introduction

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Menadione sodium sulphite (MSB) induces systemic resistance by activating redox signaling systems. The herbicide lactofen targets protoporphyrinogen oxidase, which in turn causes singlet oxygen generation. Singlet oxygen is involved in triggering ROS-mediated signaling system. Lactofen application provides significant control of fungal and oomycete diseases. Trifluralin, a dinitroaniline herbicide, induces disease resistance against several pathogens by manipulating redox signaling system. Glufosinate ammonium is a nonselective herbicide. It activates ROS-dependent SA signaling system and induces resistance against pathogens. Milsana activates ROSmediated signaling system and is highly effective in controlling powdery mildew diseases in crop plants. β-Aminobutyric Acid (BABA) has been shown to induce disease resistance against various pathogens by triggering ROS production. Potassium dihydrogen phosphate induces systemic resistance by inducing a rapid generation of superoxide and hydrogen peroxide. Silicon is another potential tool to enhance defense responses by activating ROS signaling system. Manipulation of nitric oxide (NO) signaling by sodium nitroprusside (SNP) may be another potential approach to trigger plant immune system for effective crop management. Treatment of plants with BTH triggers SA signaling and causes the induction of a unique physiological state called “priming”. BTH activates SA-dependent SAR in many crops and has been found to be useful in management of several crop diseases caused by oomycetes, fungi, bacteria, and viruses. N-cyanomethyl-2-chloroisonicotinamide (NCI) is another potential chemical that activates NPR1-dependent SA signaling system. CMPA (3-chloro-1-methyl-1H-pyrazole-5-carboxylic acid) is another compound, which activates SA signaling pathway. Tiadinil (3,4-dichloro-N-(2cyanophenyl)-1,2-thiazole-5-carboxamide) is another potential chemical, which triggers SA signaling pathway by activating NPR1 gene expression. Probenazole and its metabolite BIT intervene in SA signaling system at SA accumulation stage as well as at NPR1 stage to trigger resistance against pathogens. BABA induces priming in the SAR induction pathway. The descendants of primed plants exhibit next-generation systemic acquired resistance. Azelaic acid stimulates the production of AZ11, a protein which helps prime the plant to build up its immunity by generating additional SA. An oligosaccharide product obtained from burdock (Arctium lappa) plant triggers production of methyl salicylate involved in SA signaling system and confers disease resistance. Yeast elicitor treatment activates SA signaling system and induces resistance against oomycete, fungal, and bacterial pathogens in many crop plants. Priming for JA-dependent defenses using hexanoic acid appears to be an effective tool for management of crop diseases. Ulvan is a potential activator of JA signaling pathway. Alkamides are fatty acid amides, which are commonly present in plants. N-isobutyl decanamide, the most highly active alkamide, has been shown to be a potential tool to manipulate enzymes involved in JA biosynthesis pathway. SA, JA, and ethylene signaling systems can be activated by using different rhizobacteria and the rhizobacteria trigger “induced systemic resistance”. Keywords Ca2+ ion channels · H+ - ATPase proton pump · Annexin · G-protein genes · ROS · NO · MAPK · NPR1 · gene · Chitosan · Laminarin · Thiamine · BABA · BTH · Probenazole · SAR · ISR

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1.1 Signals and Signaling Systems Involved in Activation of Plant Innate Immune System Plants are endowed with innate immune system, which has a high potential to detect and fight against viral, bacterial, oomycete, and fungal pathogens and protect the crop plants against wide range of diseases (Vidhyasekaran 2002, 2004, 2007a, b, 2014, 2015, 2016). The plant innate immune system is a sleeping system in unstressed healthy plants (Vidhyasekaran 2014). Specific signals are needed to activate the “sleeping” immune system. My earlier books (Vidhyasekaran 2014, 2015, 2016) described in detail the various signals and signaling systems involved in activating the sleeping giant. The first book (Vidhyasekaran 2014) describes the function of pathogen-associated molecular patterns (PAMPs)/Microbe-associated molecular patterns (MAMPs) as primary signals involved in activation of the sleeping plant immune system. PAMPs directly bind to plant pattern recognition receptors (PRRs) and the PAMP-PRR complex activates the plant immune system. This book (Vidhyasekaran 2014) describes the PAMP-PRR signaling complex and signal transduction system. Several second messengers are involved in delivering the information generated by the PAMP-PRR signaling complex to the proteins which decode/interpret signals to initiate defense gene expression. Calcium ion is an important second messenger. Calcium signatures are recognized by calcium sensors to transduce calcium-mediated signals into downstream events. G-proteins act as molecular switches in signal transduction system. MAPK cascades transduce extracellular stimuli into intracellular responses. Reactive oxygen species (ROS) and nitric oxide (NO) also act as second messengers in transmitting the PAMP signal (Vidhyasekaran 2014). My second book (Vidhyasekaran 2015) describes plant hormone signaling systems including salicylate (SA), jasmonate (JA), ethylene (ET), abscisic acid (ABA), auxins, gibberellins, and brassinosteroids signaling systems involved in activation of the sleeping immune systems. Two forms of induced resistance, systemic acquired resistance (SAR) and induced systemic resistance (ISR) are recognized. SA signaling system is involved in SAR, while JA/ET signaling system is involved in ISR. This book (Vidhyasekaran 2015) also describes the plant hormones-modulated priming, histone memory for information storage gene priming, chromatin remodeling in priming, DNA methylation in trans-generational SAR, mobile signal complex, signal receptor complex, JAZ proteins, cross-talk between hormones, and phosphorelay signaling systems. My third book (Vidhyasekaran 2016) describes various bioengineering and molecular manipulation techniques to switch on PAMP-PRR signaling complex. Early and robust activation of PAMP-PRR signaling complex triggers strong defense responses. Bioengineering PRRs is a potential technology to awaken the quiescent plant innate immunity for effective management of crop diseases. The present book describes various bioengineering and molecular manipulation techniques to activale calcium ion influx–mediated immune signaling system, reactive oxygen species, redox and nitric oxide signaling systems, MAPK signal transduction system, SA, JA, and ET signaling systems for crop disease management.

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1.2 Bioengineering Technologies to Activate Plant Immunity Signaling Systems for Management of Crop Diseases Plant innate immunity can be activated by different biotic or abiotic elicitor signals (Vidhyasekaran 2014). The plant immune system uses several second messengers to encode information generated by biotic or abiotic elicitors and deliver the information to proteins which decode/interpret signals and initiate defense gene expression (Hwang and Hwang 2011; Vidhyasekaran 2014). Calcium ion is an important intracellular second messenger. It acts as a signal carrier and the calcium signaling is modulated by specific “calcium signatures”. These calcium signatures result from the concerted action of channels, pumps, and carriers that shape temporally and spatially defined Ca2+ elevations (Vidhyasekaran 2014). Cellular Ca2+ signals are decoded and transmitted by a tool kit of Ca2+ binding proteins that relay this information into downstream responses (Vidhyasekaran 2014). Several genes involved in the calcium ion influx–mediated immune signaling system have been exploited for management of crop diseases. Genes encoding calmodulin-binding protein (Wan et al. 2012), G-proteins (Li et al. 2005; Thao et al. 2007), glutamate receptor-like ion channel protein (Kang et al. 2006), H+ -ATPase proton pump (Abad et al. 1997; Pontier et al. 2002), calcium dependent protein kinase (CDPK) (Geng et al. 2013), and annexin (Jami et al. 2008) have been bioengineered to develop disease-resistant plants. ROS signaling network plays a central role in launching the defense response (Vidhyasekaran 2014). NPR1, the transcriptional regulatory cofactor, is activated by redox signaling in plants and NPR1 is involved in triggering defense responses. NPR1 gene has been used to develop transgenic plants using bioengineering technologies (Chern et al. 2001; Friedrich et al. 2001; Makandar et al. 2006). Cysteinerich receptor-like kinases (CRKs) are connected to redox and ROS signaling (Vidhyasekaran 2014). Transgenic plants overexpressing CRK genes show enhanced disease resistance by triggering enhanced ROS production (Bourdais et al. 2015; Yeh et al. 2015). L-type lectin receptor kinases (LecRKs) have been exploited to develop transgenic disease-resistant plants. These transgenic plants show enhanced production of ROS and trigger defense responses against pathogens (Huang et al. 2014). Peroxidases in the cell wall can generate apoplastic H2 O2 at neutral to basic pH in the presence of reductants in plant cells. It is possible to generate transgenic plants overexpressing peroxidase gene to overproduce peroxidase resulting in enhanced ROS accumulation. These transgenic plants show enhanced disease resistance (Choi et al. 2007). Super oxide dismutase gene has been engineered to activate ROS-mediated immune signaling for disease management (Guevara-Olvera et al. 2012; Rietz et al. 2012). Fungal glucose oxidase gene has been engineered to develop disease-resistant plants. Expression of the fungal glucose oxidase gene leads to elevated production of H2 O2 in the transgenic plants resulting in increased disease resistance (Felcher et al. 2003; Maruthasalam et al. 2010). Nitric oxide (NO) signaling system can also be manipulated for disease management. GSNOR (S-nitroso glutathione reductase)

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has been exploited using antisense strategy to develop transgenic plants expressing resistance against oomycete and bacterial pathogens (Rustérucci et al. 2007). Nitric oxide synthase (NOS) has been used to develop transgenic plants. The mammalian NOS isolated from rat brain has been shown to be a potential tool to develop transgenic plants expressing resistance against a wide range of pathogens (Altamiranda et al. 2008; Chun et al. 2012). Mitogen-activated protein kinases (MAPKs) are important components in the plant immune signal transduction system and they transduce extracellular stimuli into intracellular transcription factors (Vidhyasekaran 2014). Technologies have been developed to utilize appropriate MAPK genes for developing disease-resistant plants. Bioengineering specific MAPK genes has been shown to induce disease resistance by triggering phosphorylation of transcription factors (Cheong et al. 2003). Some MAPK genes have been shown to regulate SA-mediated systemic acquired resistance (SAR) (Vidhyasekaran 2015). The cotton MAPK gene GhMPK7 and the maize MAPK gene ZmSIMK1 activate SA signaling system and transgenic plants overexpressing these genes show enhanced disease resistance (Shi et al. 2010; Wang et al. 2014). Some MAPK genes (BnMPK4 and MK1) trigger the JA-mediated signaling system and these genes have been exploited to develop transgenic plants expressing enhanced resistance against necrotrophic pathogens (Wang et al. 2009). The cotton MAPK genes GhMPK16 and GHMPK2 activate SA, JA and ET signaling complex and these genes have been engineered to develop disease-resistant transgenic plants (Zhang et al. 2011). Some mitogen-activated protein kinase kinase (MAPKK) genes have also been exploited to activate immune responses for crop disease management (Shen et al. 2010). Some MAPK genes negatively regulate the defense responses and these genes also have been exploited to develop disease-resistant plants by knocking-out these MAPK genes (Liu et al. 2011). MAPK gene can also be manipulated to trigger the immune responses by using the biocontrol agent Trichoderma asperellum. A MAPK, designated as Trichoderma-induced MAPK (TIPK), has been identified and characterized in the Trichoderma- induced disease-resistant cucumber plants. The TIPK gene has been cloned and cucumber plants overexpressing the TIPK gene show resistance against pathogen (Liu et al. 2011). Salicylic acid (SA) signaling system is the most important signaling system activating plant innate immunity (Vidhyasekaran 2014, 2015, 2016). Plants do not have much endogenous SA. It has been suggested that by increasing the SA content, defense genes can be activated and diseases can be controlled (Vidhyasekaran 2015). Increased synthesis and accumulation of salicylic acid in plants result in increased expression of defense genes conferring resistance against pathogens. SA may be synthesized through the isochorismate pathway (Vidhyasekaran 2015). Isochorismate synthase (ICS) and isochorismate pyruvate lyase (IPL) are the key enzymes involved in biosynthesis of SA. SA is synthesized from chorismate, the end product of the shikimate pathway. Chorismate is converted by ICS to isochorismate, which is subsequently cleaved by IPL to yield SA (Vidhyasekaran 2015). The genes encoding ICS and IPL cloned from two different bacteria have been exploited to develop transgenic tobacco plants overexpressing both ICS and IPL genes. These transgenic plants show

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enhanced accumulation of SA. The transgenic tobacco plants which show high accumulation of SA, show enhanced disease-resistance (Verberne et al. 2000). Several SA signaling regulator proteins are involved in SA production pathway. PAD4 is a key regulator protein acting at upstream of SA. PAD4 is required for amplification of weak signals to a level sufficient for activation of SA signaling. PAD4 gene has been exploited to develop disease-resistant wheat plants (Makandar et al. 2015). RNA-binding proteins (RBP) play important roles in post-transcriptional gene regulation by controlling splicing, polyadenylation, mRNA stability, RNA trafficking, and translation (Pallas and Gomez 2013; Marondedze et al. 2016). A RBP from Arabidopsis thaliana, AtRBP-defense related 1 (AtRBP-DR1), has been shown to be involved in plant immune responses. The AtRBP-DR1 gene was cloned and exploited for developing disease-resistant plants. Transgenic Arabidopsis plants overexpressing AtRBP-DR1 were developed (Qi et al. 2010). These transgenic plants show higher mRNA levels of SID2. The SID2 gene encodes an isochorismate synthase, which is required for producing SA during immune responses (Wildermuth et al. 2001). Activation of the SA pathway by AtRBP-DR1 overexpression was fully dependent on SID2 (Qi et al. 2010). Overexpression of AtRBP-DR1 led to high accumulation of SA and these transgenic plants show enhanced resistance to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Qi et al. 2010). A camodulin binding protein, CBP60g, has been shown to be involved in activating SA biosynthesis (Wang et al. 2009; Vidhyasekaran 2015). CBP60g has been shown to bind to the promoter region of SID2 (Wang et al. 2011). Transgenic Arabidopsis plants overexpressing CBP60g gene were developed and these transgenic plants showed elevated SA accumulation and increased expression of defense genes (Wan et al. 2012). The transgenic plants showed enhanced resistance against the bacterial pathogen Pseudomonas syringae (Wan et al. 2012). Several transcription factors are known to take part in the regulation of SA signaling pathway (Vidhyasekaran 2015, 2016). The transcription factor genes OsWRKY13 (Qiu et al. 2007, Cheng et al. 2015), OsWRKY89 (Wang et al. 2007), and NtWIF (Waller et al. 2006) have been engineered to develop disease-resistant plants. Ubiquitin-proteasome pathway can be manipulated to trigger SA signaling system for crop disease management (Vidhyasekaran 2015). Transgenic tobacco plants expressing a ubiquitin-variant with Lys to Arg exchange in position 48 (ubr48) were developed (Becker et al. 1993). These transgenic tobacco plants showed enhanced resistance against Tobacco mosaic virus (Becker et al. 1993). The transgenic plants expressing the ubiquitin variant ubr78 contained elevated levels of SA compared to the control plants (Conrath et al. 1998). SGT1 genes are required for SA accumulation and they have been engineered to develop disease resistant plants (Wang et al. 2008; Zhou et al. 2008). NPR1 gene is a master regulator of the SA-mediated induction of systemic acquired resistance (SAR) (Vidhyasekaran 2015). NPR1 gene has been engineered to develop several transgenic crop plants including rice, tomato, citrus, carrot, and strawberry (Feng et al. 2011; Le Henanff et al. 2011; Chen et al. 2012; Dutt et al. 2015; Silva et al. 2015; Boscariol-Camargo et al. 2016; Molla et al. 2016; Joshi et al. 2017).

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Jasmonic acid and their derivatives (JA) are important signal molecules detected in a wide spectrum of plant species (Vidhyasekaran 2015). They are involved in activation of plant immune system. The concentrations of JA in healthy unperturbed plant tissues are very low. Increased concentrations of JA are needed to activate the plant immune system and to induce “Induced systemic resistance (ISR)”. JA concentration can be increased by enhancing the activities of the enzymes involved in JA biosynthesis. The key enzymes involved in the biosynthesis involve phospholipases, lipoxygenases (LOXs), allene oxide synhases (AOS), allene oxide cyclase (AOC), and OPDA reductase (OPR) (Vidhyasekaran 2015). The genes encoding these enzymes have been cloned and engineered to enhance the JA biosynthesis and JA accumulation activates plant immune system (Mei et al. 2006; Mene-Saffrané et al. 2003; Hwang and Hwang 2010; Hou et al. 2018). The transcription factor genes OsMYC2 and VvWRKY1 have been engineered to manipulate JA signaling system for crop disease management (Marchive et al. 2013; Uji et al. 2016). Under natural conditions endogenous ethylene content is very low in plants and its level is not sufficient to induce defense gene expression (Vidhyasekaran 2015; Ravanbakhsh et al. 2018). Increase in ethylene biosynthesis induces enhanced defense responses. Hence several attempts were made to induce ethylene biosynthesis in plants for disease management. Transgenic rice lines overexpressing ACC synthase gene, OsACS2, have been generated and these transgenic plants show increased levels of endogenous ethylene. The transgenic lines overexpressing OsACS2 show increased resistance to the rice blast pathogen Magnaporthe oryzae and the rice sheath blight pathogen Rhizoctonia solani (Helliwell et al. 2013). ERF belonging to the APETELA2 (AP2)/ETHYLENE RESPONSIVE ELEMENT BINDING PROTEIN (EREBP) transcription factor family is the important group of transcription factors functioning downstream in ethylene signaling system (Vidhyasekaran 2016). Several ERF genes have been engineered to develop diseaseresistant plants (Dong et al. 2015; Xing et al. 2017; Wang et al. 2018). EIN2 is a membrane protein that acts as the central regulator of ethylene signaling pathways. The rice plants overexpressing OsEIN2 show enhanced resistance against the rice blast pathogen Magnaporthe oryzae (Yang et al. 2017).

1.3 Molecular Manipulation of Plant Immunity Signaling Systems Using Abiotic or Biotic Elicitors for Management of Crop Diseases Several biotic and abiotic elicitors have been developed as commercial formulations to activate the plant immune system and induce disease resistance. Chitosan has been found to be highly effective in inducing resistance against oomycete, fungal, viral, and bacterial diseases (Algam et al. 2010; El-Mohamedy et al. 2014; Sunpapao and Ponsuriya 2014). Chitosan treatment inactivates H+ -ATPase resulting in membrane depolarization, which is involved in increasing Ca2+ influx (Amborabé et al. 2008).

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Thiamine treatment triggers Ca2+ influx and induces Ca2+ -induced protein kinase C (PKC) activity. Thiamine treatment effectively controls bacterial, fungal, and viral diseases of crop plants by activating Ca2+ signaling system (Ahn et al. 2005). Many attempts have been made to manipulate the ROS signaling system to trigger host defense responses. BTH (benzo[1,2,3]thiadiazole-7-carbothioc acid S-methyl ester) is the most successfully developed commercial compound to manipulate ROS signaling system for management of viral, bacterial, and phytoplasma diseases and parasitic plants, which are difficult to be controlled by traditional chemical control methods (Walters et al. 2005; Mandal et al. 2008). BTH induces accumulation of ROS through activation of different signaling pathways (Faize et al. 2004; Cavalcanti et al. 2006; Lanteri et al. 2008). The induced ROS triggers several downstream events inducing expression of several defense genes (Faize et al. 2004; Deepak et al. 2006; Faoro et al. 2008; Schreiber and Desveaux 2008). BTH has been shown to induce several genes with potential roles in establishing reducing conditions following the oxidative burst induced by it (Faize et al. 2004; Deepak et al. 2006; Faoro et al. 2008). Thiol-based redox signaling has been suggested to contribute to the activation of a primed state in BTH-treated plants (Ku˙zniak et al. 2014). BTH treatment, which induces redox conditions, activates NPR1 (for non-expresser of PR gene 1) and induces resistance against pathogens (Chern et al. 2001; Zhu et al. 2003). NPR1 gene is a master regulator of the systemic acquired resistance (SAR) in plants. NPR1 enhances the binding of transcription factors to the promoters of pathogenesis-related (PR) defense genes for activation (Chern et al. 2008; Mukherjee et al. 2010). BTH may activate the plant immune system by triggering accumulation of ROS, which may enhance the expression of NPR1, the key regulator of the long-lasting broad-spectrum defense responses. BTH treatment effectively controls several fungal, oomycete, bacterial, phytoplasma, and viral diseases in wheat, rice, barley, potato, bean, cucumber, lettuce, sunflower, oilseed rape, sugarcane, strawberry, Japanese pear, sugarbeet, blackgram, red clover and chrysanthemum (D’Amelio et al. 2010; Venkatesan et al. 2010; Romanazzi et al. 2013; Oliveira and Nishijima 2014). Riboflavin is another compound which can be used to manipulate ROS and redox signaling system (Dong and Beer 2000). It induces H2 O2 production. Riboflavin induces priming of defense responses and triggers systemic resistance against pathogens (Saikia et al. 2006). Menadione sodium sulphite (MSB) is a water-soluble addition compound of vitamin K3 . It is a ROS generator, readily undergoing cellmediated one-electron reduction, producing superoxide radicals (O2 − ) and H2 O2 (Hassan and Fridovich 1979). MSB treatment induces systemic resistance by activating redox signaling systems (Borges-Pérez and Fernandez-Falcon 1996). Some herbicides have been shown to act as plant innate immunity system activators. The herbicide lactofen targets protoporphyrinogen oxidase, which in turn causes singlet oxygen generation. Singlet oxygen is involved in triggering ROS-mediated signaling system. Lactofen application provides significant control of fungal and oomycete diseases (Graham 2005). Trifluralin, a dinitroaniline herbicide, induces disease resistance against several pathogens by manipulating redox signaling system (Bolter et al. 1993). Glufosinate ammonium is a nonselective herbicide. It activates ROS-dependent SA signaling system and induces resistance against pathogens (Ahn

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2008). Milsana (Reynoutria sachalinensis formulation) activates ROS-mediated signaling system and is highly effective in controlling powdery mildew diseases in crop plants (Randoux et al. 2006). β-Aminobutyric Acid (BABA) has been shown to induce disease resistance against various pathogens by triggering ROS production. BABA-induced resistance is mostly based on priming of defense responses rather than on the direct activation of these defense responses. BABA has been shown to prime RbohD gene, which encodes a NADPH oxidase potentially involved in ROS production (Dubreuil-Maurizi et al. 2010; Pastor et al. 2013). Potassium dihydrogen phosphate induces systemic resistance by inducing a rapid generation of superoxide and hydrogen peroxide (Orober et al. 2002). Potassium phosphonate triggers ROS signaling system–mediated plant defense responses by rapidly releasing superoxide around the point of infection (Daniel and Guest 2006). Oxycom is a commercially available chemical containing reactive oxygen species. It acts as a plant innate immunity activator. Applications of Oxycom triggers plant immune system downstream of ROS (Blee et al. 2004). Several bacterial and fungal biocontrol agents have been shown to induce systemic resistance (ISR) against several plant pathogens in various crop plants. Some of the rhizobacteria activate the plant innate immune system by triggering the ROS signaling system. Pseudomonas fluorescens WCS374 is a potential tool to trigger ROS signaling system and confer resistance against pathogens (De Vleesschauwer et al. 2008). Serratia plymuthica ICI270, primes leaves for enhanced attacker-induced accumulation of ROS. It induces accumulation of ROS in leaves and induces systemic resistance (De Vleesschauwer and Höfte 2009). Bacillus mycoides elicits ISR by triggering ROS production. Silicon is another potential tool to enhance defense responses by activating ROS signaling system (De Vleesschauwer et al. 2009). Silicon treatment significantly alters the activity of lipoxygenase (LOX), which catalyzes the direct oxygenation of polyunsaturated fatty acids and produces O2 – . Several silicon-based formulations are available for management of crop diseases (Sun et al. 2010). Manipulation of nitric oxide (NO) signaling by sodium nitroprusside (SNP) may be another potential approach to trigger plant immune system for effective crop management. SNP is a NO generator (Kobeasy et al. 2011; Thuong et al. 2015). SNP treatment triggered ROS and SA signaling systems (Thuong et al. 2015). Sodium nitroprusside applied as foliar spray effectively triggered host defense responses against Peanut mottle virus in peanut (Kobeasy et al. 2011). Treatment of plants with BTH triggers SA signaling and causes the induction of a unique physiological state called “priming” (Camañes et al. 2012; Slaughter et al. 2012) BTH induces histone modifications, which may be involved in the gene priming (Jaskiewicz et al. 2011). The expression of the WRKY genes is enhanced in BTH-treated plants. BTH triggers NPR1-dependent chromatin modification on WRKY promoters to activate defense gene expression (Jaskiewicz et al. 2011). BTH activates SA-dependent SAR in many crops and has been found to be useful in management of several crop diseases caused by oomycetes, fungi, bacteria, and viruses. N-cyanomethyl-2-chloroisonicotinamide (NCI) is another potential chemical that activates NPR1-dependent SA signaling system. NCI activates SAR by stimulating the site between SA and NPR1. NCI has been found to be effective in inducing

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resistance against Tobacco mosaic virus (TMV), P. syringae pv. tabaci, and Oidium lycopersici in tobacco and Magnaporthe oryzae in rice (Nakashita et al. 2002; Yasuda 2007). CMPA (3-chloro-1-methyl-1H-pyrazole-5-carboxylic acid) is another compound, which activates SA signaling pathway. It acts in the SA signaling pathway between SA production and NPR1 activity. It protects rice from infection by rice blast pathogen Magnaporthe oryzae and bacterial blight pathogen Xanthomonas oryzae pv. oryzae. It enhances resistance of tobacco to Pseudomonas syringae pv. tabaci and Oidium sp. (Nakashita et al. 2003; Nishioka et al. 2005; Yasuda et al. 2003). Tiadinil (3,4-dichloro-N-(2-cyanophenyl)-1,2-thiazole-5-carboxamide) is another potential chemical, which triggers SA signaling pathway by activating NPR1 gene expression. It induces resistance against various fungal, bacterial, and viral diseases in tobacco and is practically used to control rice blast disease (Yasuda et al. 2004, 2006; Yasuda 2007). Probenazole (3-allyloxy-1,2-benzisothiazole-1,1-dioxide) and its metabolite 1,2-benzisothiazole-3 (2H)-one 1,1-dioxide (BIT, saccharin) are potential plant defense activators and both of them are known to induce SA accumulation and activate SA signaling system (Schreiber and Desveaux 2008). Probenazole/BIT intervenes in SA signaling system at SA accumulation stage as well as at NPR1 stage to trigger resistance against pathogens (Yoshioka et al. 2001; Park et al. 2007, 2009). The nonprotein amino acid β-aminobutyric acid (BABA) induces broad-spectrum resistance in a range of crops. BABA induces priming in the SAR induction pathway. The descendants of primed plants exhibit next-generation systemic acquired resistance (Slaughter et al. 2012). SA signaling system can also be activated using plant-derived products. Azelaic acid, a natural compound found in several plants, is a signal molecule triggering plant defense responses. Azelaic acid does not directly induce defense responses, but confers on the plants the ability to mount a faster and stronger defense response if and when the plant is attacked again. It does this by increasing the production of SA. Azelaic acid stimulates the production of AZ11, a protein which helps prime the plant to build up its immunity by generating additional SA (Jung et al. 2009). AHO (3-acetonyl-3-hydroxyoxindole) isolated from the extracts of Strobilanthes cusia is an activator of SA signaling system. When tobacco plants are treated with AHO, SA accumulates in the leaf tissues and induces disease resistance (Li et al. 2008). An oligosaccharide product obtained from burdock (Arctium lappa) plant triggers production of methyl salicylate involved in SA signaling system and confers disease resistance (He et al. 2006). N-Acyl-L-homoserine lactones (AHLs)–producing bacteria, which induce SA-dependent systemic resistance, have been shown to be potential tools for management of crop diseases (Schuhegger et al. 2006). Some of the rhizobacterial strains activate the plant innate immune system by triggering SA signaling system and they are widely used for management of crop diseases (De Meyer et al. 1999; Zhang et al. 2002; Tjamos et al. 2005). SA signaling system can be activated by some MAMPs (for Microbe-associated molecular patterns) for effective crop disease management. The MAMP yeast elicitor treatment activates SA signaling system and induces resistance against oomycete, fungal, and bacterial pathogens in many crop plants (Raacke et al. 2006; Tosun 2007).

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Hexanoic acid is a nine carbon dicarboxylic acid that acts as an inducer of plant defenses by means of a priming mechanism (Vicedo et al. 2009). Priming results in a faster and stronger induction of defense mechanisms after pathogen attack (Conrath 2011; Po-Wen et al. 2013). Hexanoic acid primes JA biosynthesis pathway (Vicedo et al. 2009). Priming for JA-dependent defenses using hexanoic acid appears to be an effective tool for management of crop diseases (Djami-Tchatchou et al. 2017). Ulvan, a sulfated polysaccharide product isolated from green algae belonging to the Ulva genus is a potential activator of JA signaling pathway (Jaulneau et al. 2010). Ulvan treatment induces elevation of JA content in Medicago truncatula. It also induces the expression of well-known jasmonic acid-responsive genes including lipoxygenase, hydroxyproline-rich glycoproteins, proline-rich proteins, defensin and wound-induced protein (Jaulneau et al. 2010). Ulvan treatment induces biosynthesis of jasmonoyl-isoleucine (Staswick and Tiryaki 2004), which is involved in defense signaling (Wasternack and Hause 2013). Ulvan spraying has been shown to control several foliar diseases (de Freitas and Stadnik 2012, 2015; de Freitas et al. 2015). Alkamides are fatty acid amides, which are commonly present in plants (MéndezBravo et al. 2011). N-isobutyl decanamide, the most highly active alkamide, has been shown to be a potential tool to manipulate enzymes involved in JA biosynthesis pathway. Alkamide treatment enhances the expression of genes encoding enzymes for jasmonic acid biosynthesis. It enhances the expression of lipoxygenase genes (LOX2 and LOX3), allene oxide synthase gene (AOS), allene oxide cyclase2 gene (AOC2), and OPDA reductase3 (OPR3) gene. The alkamide has great potential to combat pathogens by triggering JA biosynthesis pathway (Méndez-Bravo et al. 2011). Chitosan has been developed as a potential activator of JA signaling system to induce defense responses for crop disease management (Bueter et al. 2013). Chitosan triggers lipoxygenase activity and induces accumulation of jasmonic acid (Doares et al. 1995; Rakwal et al. 2002). Chitosan activates plant innate immune system and controls several crop diseases (Prapagdee et al. 2007; Li et al. 2009; Dafermos et al. 2012). JA signaling system can be manipulated using some microbes for crop disease management. Trichoderma spp. are known to be involved in triggering ‘induced systemic resistance’ (ISR) in many plants (Harman et al. 2004; Vidhyasekaran 2004; Shoresh et al. 2010: Mathys et al. 2012; Martinez-Medina et al. 2013; Harel et al. 2014). Trichoderma asperellum T 203 induced systemic resistance against the foliar bacterial pathogen Pseudomonas syringae pv. lachrymans and reduced the angular leaf spot symptom development (Yedidia et al. 2003). The Trichoderma strain induced the expression of Lox1 encoding lipoxygenase (LOX), the key enzyme in LOX pathway which is involved in biosynthesis of JA (Shoresh et al. 2005). It also induced the lipoxygenase pathway gene encoding hydroperoxide lyase (HPL) (Yedidia et al. 2003). Trichoderma virens is a commercially formulated biocontrol agent and it is effective in the control of Rhizoctonia solani, Sclerotium rolfsii, and Pythium spp. in several crop plants (Mukherjee and Kenerley 2010). It induces resistance against several crop diseases by activating JA signaling system (Djonovic et al. 2006). Pseudomonas putida strain BTP1 treatment primes tomato plants to activate two key enzymes of lipoxygenase (LOX) pathway, lipoxygenase (LOX) and

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lipid hydroperoxidase (LHP) after challenge inoculation with the pathogen Botrytis cinerea (Akram et al. 2008). P. putida BTP1 induces ISR in bean against the gray mold pathogen B. cinerea (Ongena et al. 2002) and in cucumber against the root rot oomycete pathogen Pythium aphanidermatum (Ongena et al. 1999, 2000). Ethylene signaling system can be activated by using different rhizobacteria (Leeman et al. 1995a, b; Ran et al. 2005a, b; Spencer et al. 2003). Trichoderma asperellum triggers ISR against several pathogens. Ethylene signal transduction pathway has been shown to be involved in the ISR induced by T. asperellum (Shoresh et al. 2005). Pythium oligandrum is a biocontrol agent which controls several soil-borne fungal and bacterial pathogens (Benhamou et al. 1997; Picard et al. 2000; Takenaka et al. 2003; Hase et al. 2006). P. oligandrum treatment induces biosynthesis of ethylene (Hase et al. 2006). P. oligandrum also activates ethylene signaling pathway. Activation of the ethylene-dependent signaling pathway is accompanied by increased expression of genes encoding ethylene receptors and ethylene-responsive transcription factors (Hase et al. 2006). Collectively these studies suggest that enhancing disease resistance through altered regulation of plant immune signaling systems will be an attractive technology for management of crop diseases.

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Chapter 2

Manipulation of Calcium Ion Influx—Mediated Immune Signaling Systems for Crop Disease Management

Abstract Calcium ion is the principal mediator in plant immune signaling system. Ca2+ signaling system involves calcium signatures, which result from the concerted action of voltage-dependent Ca2+ -permeable ion channels, cyclic nucleotide-gated channels, glutamate receptor-like ion channels, calcium transporters, calcium ion pumps, carriers, and Ca2+ efflux channels, The Ca2+ signaling system involves Ca2+ sensors. Calmodulins (CaMs) and CaM-like proteins (CMLs) are calcium sensors. Cellular Ca2+ signals are decoded and transmitted by Ca2+ binding proteins that relay this information into downstream responses. Calcium-dependent protein kinases (CDPKs) perceive Ca2+ signals nd relay them into specific phosphorylation events to induce downstream defense responses. Early and rapid induction of Ca2+ signaling system has been shown to be necessary for switching on host defense responses to prevent the invading pathogen development. Manipulation of even one component in the Ca2+ signaling system may be able to trigger the entire gamut of immune response signaling systems to confer resistance against a wide-spectrum of pathogens. Gproteins are involved in initiating Ca2+ influx. Genes encoding G-proteins have been cloned and used for engineering to develop disease resistant plants. Bioengineering gene encoding glutamate receptor-like ion channel protein has been found to be a useful technology to develop disease resistant plants. Manipulation of the H+ -ATPase proton pump has been shown to be a potential tool for management of crop diseases. The enzyme transports one H+ in exchange of one K+ . The K+ /H+ exchange response may be mediated by Ca2+ influx. The algal elicitor laminarin manipulates the proton pump and triggers defense responses. Several commercial formulations of laminarin have been developed to control oomycete, fungal, and bacterial pathogens in monocot and dicot plants. Chitosan formulations inactivate H+ -ATPase resulting in membrane depolarization, which is involved in increasing Ca2+ influx. Chitosan effectively controls various oomycete, fungal, bacterial and viral diseases. Plant annexins are capable of mediating passive, channel-like Ca2+ transport and Ca2+ influx. Transgenic plants ectopically expressing annexin gene show enhanced disease resistance. Calmodulin (CaM) is a Ca2+ sensor protein and several disease-resistant plants have been developed by engineering calmodulin genes. Engineering calmodulin-binding proteins also have been shown to be effective in developing disease-resistant plants. Calcium-dependent protein kinases (CDPKs) are Ca2+ sensor proteins in transducing differential Ca2+ signatures activating complex downstream responses. Disease © Springer Nature B.V. 2020 P. Vidhyasekaran, Plant Innate Immunity Signals and Signaling Systems, Signaling and Communication in Plants, https://doi.org/10.1007/978-94-024-1940-5_2

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resistant plants against wide range of pathogens could be developed using CDPK genes. Thiamine (vitamin B1) is involved in priming of plants to induce disease resistance. It provides long-lasting protection against pathogens. Thiamine triggers Ca2+ influx-dependent signaling pathway. Thus, manipulation of Ca2+ -influx-dependent signaling pathways is a potential tool for management of various crop diseases. Keywords Ca2+ sensors · G-proteins · Laminarin · Membrane depolarization · Annexins · Calmodulin · CDPK genes · Thiamine

2.1 Ca2+ Signaling Components Calcium is commonly involved as intracellular messenger in the transduction of PAMP (pathogen-associated molecular pattern) signals in plant immune signaling system (Navazio et al. 2007; Kudla et al. 2010; Kwaaitaal et al. 2011; Vidhyasekaran 2014). Ca2+ signals are represented by stimulus-specific signatures called “calcium signatures” that result from the concerted action of channels, pumps, and carriers that shape temporally and spatially defined Ca2+ elevations (Fig. 2.1; Kang et al. 2006; Lecourieux et al. 2006; Kudla et al. 2010; Hamada et al. 2012; Price et al. 2012; Kurusu et al. 2013; Forde and Roberts 2014; Vidhyasekaran 2014). Cellular changes in Ca2+ in response to diverse signals are recognized by protein sensors. Calmodulins (CaMs) and CaM-like proteins (CMLs) are calcium sensors that have no enzymatic activity of their own but upon binding Ca2+ interact and modulate the activity of other proteins involved in a large number of plant processes (Reddy et al. 2011; Leba et al. 2012; Vidhyasekaran 2014). Plant annexins are Ca2+ -dependent phospholipid-binding proteins (Jami et al. 2012). Cellular Ca2+ signals are decoded and transmitted by a toolkit of Ca2+ binding proteins that relay this information into downstream responses (Dodd et al. 2010; Kudla et al. 2010; Vidhyasekaran 2014). Major transduction routes of Ca2+ signaling involve Ca2+ -regulated kinases mediating phosphorylation events that orchestrate downstream responses or comprise regulation of gene expression via Ca2+ -regulated transcription factors and Ca2+ -responsive promoter elements (Kudla et al. 2010). Calcium-dependent protein kinases (CDPKs) are multifunctional proteins in which a calmodulin-like calcium sensor and a protein kinase effector domain are combined in one molecule (Romeis and Herde 2014; Vidhyasekaran 2014). CDPKs are primarily recognized as signaling mediators, which perceive rapid intracellular changes of Ca2+ concentration, triggered by various PAMPs, and relay them into specific phosphorylation events to induce downstream defense responses (Vidhyasekaran 2014).

2.1 Ca2+ Signaling Components

25 Initiation and regulation of Ca2+ influx: G-proteins Ca2+ Influx Channels: Depolarization-activated Ca2+-Permeable Channels Hyperpolaization-activated Ca2+-Permeable Channels Cyclic Nucleotide-Gated Ion Channels Glutamate Receptor-Like Ion Channels Ca2+-permeable transporter -Annexins

Ca2+ Efflux Channels: Inositol 1,4,5-Trisphosphate-Activated Ca2+ Channels cADPR Gated Channels Calcium

Slowly Acting Vacuolar (SV) Channels

Signaling

NAADP-Activated Ca2+ Efflux Channels

System Components

ATP-Fuelled Ca2+ Pumps: Ca2+-ATPases H2+-ATPases

Ca2+ Carriers: H+/Ca2+ antiporters

Ca2+ Sensors: Calmodulins, Calmodulin-like proteins, Calcineurin B-like proteins, Calcium-dependent protein kinases, Calcium-calmodulin-dependent kinases, NADPH oxidase, Copines, Phospholipase D

Fig. 2.1 Ca2+ signaling system components involved in triggering plant immune responses

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2.2 Bioengineering G-Proteins for Plant Disease Management Guanosine triphosphate (GTP)-binding proteins (G-proteins) are the regulatory GTPases, which act as molecular switches in signal transduction system (Zhang et al. 2011, 2012; Vidhyasekaran 2014). G-proteins trigger transient changes in permeability of the plasma membrane to Ca2+ and influx of extracellular Ca2+ through the membrane (Laohavisit et al. 2009, 2010; Vadassery and Oelm¯uller 2009; Vidhyasekaran 2014). G-protein activates Ca2+ channels and enhances Ca2+ influx through Ca2+ permeable channels (Wang et al. 2001; Zhang et al. 2011). G-proteins trigger changes in cytosolic Ca2+ concentrations (Blumwald et al. 1998; Schultheiss et al. 2003). The induced calcium ([Ca2+ ]cyt ) elevations predominantly result from a continuous Ca2+ influx through the plasma membrane (Hu et al. 2004; Vandelle et al. 2006). The G-proteins induce Ca2+ channel opening in plants (Gelli et al. 1997; Vidhyasekaran 2014). Protein phosphorylation precedes Ca2+ influx in tobacco cells (Tavernier et al. 1995) and the G-proteins modulate the phosphorylation system in the plasma membrane of tomato (Vera-Estrella et al. 1994b) and tobacco cells (Gerber et al. 2006). The Arabidopsis G-protein GPA1 has been demonstrated to be involved in the regulation of inward K+ channels and slow anion channels (Wu and Assmann 1994; Wang et al. 2001; Zhang et al. 2008). RACK1 is an interactor with the G-protein Rac1 in rice and RACK1 homologs have been isolated from several plant species (Shirasu and Schulze-Lefert 2003; Vidhyasekaran 2014). RACK1 binds inositol 1,4,5-trisphosphate (InsP3) receptors and regulates Ca2+ release by enhancing InsP3 receptor binding affinity for InsP3 (Patterson et al. 2004). InsP3-activated Ca2+ channel is the important Ca2+ release channel (Alexandre and Lassales 1992). InsP3-gated channels release Ca2+ from the vacuole and endoplasmic reticulum (ER) (Berridge 1993). The calcium released through this channel induces calcium waves and oscillations (calcium signatures) in the cytosol (Berridge 1993; Vidhyasekaran 2014). These results suggest that Gproteins trigger the InsP3-activated Ca2+ channel and modulates Ca2+ signature— mediated immune signaling system. G-proteins also stimulate the plasma membrane H+ -ATPase (Vera-Estrella et al. 1994b; Xing et al. 1997; Blumwald et al. 1998; Vidhyasekaran 2014). Plasma membrane H+ -ATPases generate an H+ -gradient across the plant plasma membrane. The concomitant hyperpolarization of the membrane potential induces the opening of the Ca2+ channel. The proton gradient creates an electrical potential, which drives Ca2+ uptake through ion channels (Palmgren and Harper 1999). The results suggest that the G-proteins may also modulate the expression of H+ -ATPase and activate Ca2+ signaling. Protein phosphorylation precedes Ca2+ influx in tobacco cells treated with a PAMP isolated from the oomycete pathogen Phytophthora cryptogea (Tavernier et al. 1995). The G-proteins modulate the phosphorylation/dephosphorylation system in the plasma membrane of tomato cells and transduce the signal (Vera-Estrella et al. 1994b). Phosphorylation of proteins involved in G-protein coupled signaling has been reported in tobacco cells (Gerber et al. 2006).

2.2 Bioengineering G-Proteins for Plant Disease Management

27

G-proteins trigger transient changes in permeability of the plasma membrane to Ca2+ and influx of extracellular Ca2+ through the membrane (Laohavisit et al. 2009, 2010; Vadassery and Oelm¯uller 2009). G-protein activates Ca2+ channels and enhances Ca2+ influx through Ca2+ -permeable channels. G-proteins induce Ca2+ channel opening in plants (Gelli et al. 1997). InsP3-activated Ca2+ channel is the important Ca2+ release channel, G-proteins trigger the InsP3-activated Ca2+ channel and modulates Ca2+ signature—mediated immune signaling system. Genes whose deduced amino acids sequences are similar to those of the Rho/Rac family of small GTP-binding proteins have been cloned and used for engineering to develop disease resistant plants (Kawasaki et al. 1999; Li et al. 2005). The genes encoding Rac small G-proteins have been exploited to develop transgenic plants expressing enhanced resistance against bacterial, fungal, and viral diseases. GbRac1 gene was cloned from Gossypium barbadense. A plant constitutive expression vector pRac harbouring GbRac1 was constructed and transgenic tobacco plants expressing the cotton GbRac1 gene were developed. The transgenic tobacco plants showed enhanced resistance against the fungal pathogen Alternaria alternata (Li et al. 2005). The results suggest that GbRac1 gene might have potential application in the genetic engineering of plants with enhanced disease resistance. A rab/ypt-related gene, rgp1, encoding a Ras-related small GTP binding protein has been isolated from rice. Transgenic tobacco plants expressing rgp1 gene from rice were developed. The transgenic tobacco plants conferred a high level of resistance against Tobacco mosaic virus infection (Fig. 2.2; Sano et al. 1994). The diseaseresistant plants showed accumulation of salicylic acid and increased expression of PR proteins (Sano et al. 1994). OsRac1, a rice homolog of mammalian RacGTPase has been cloned and transgenic rice plants constitutively expressing OsRac1 have been developed (Ono et al. 2001). The transgenic plants showed enhanced resistance to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Fig. 2.3; Ono et al. 2001). These plants also showed resistance against the rice blast pathogen Magnaporthe oryzae (Thao

Diameter of local lesion (mm2)

2.5

2

1.5

1

0.5

0

Wild-type plants

Transgenic plants expressing Gprotein gene

Fig. 2.2 Transgenic tobacco plants expressing rgp1 gene show enhanced resistance against Tobacco mosaic virus (Adapted from Sano et al. 1994)

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2 Manipulation of Calcium Ion Influx … 8 7

Lesion length (cm)

6 5 4 3 2 1 0

Wild-type plants

Transgenic rice plants expressing OsRac1 gene

Fig. 2.3 Transgenic rice plants expressing OsRac1 show resistance against the bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Adapted from Ono et al. 2001)

et al. 2007). The levels of the phytoalexin momilactone A were highly elevated in the transgenic plants, and the increases were 19–180-fold higher than the levels of the untransformed control plants (Ono et al. 2001). Collectively, these results suggest that engineering genes encoding G-proteins may be a useful crop disease management technology.

2.3 Engineering Glutamate-Gated Ca2+ Channel for Plant Disease Management Glutamate receptors (GLRs) comprise a glutamate-gated calcium-permeable ion channel in the plant plasma membrane (Kang et al. 2006; Vatsa et al. 2011; Price et al. 2012; Vincill et al. 2012; Manzoor et al. 2013; Vidhyasekaran 2014). Twenty glutamate receptor-like channels have been detected in Arabidopsis thaliana genome (Wheeler and Brownlee 2008). GLRs are intimately associated with Ca2+ influx and they are partly involved in free cytosolic Ca2+ variations ([Ca2+ ]cyt ) (Manzoor et al. 2013). A gene (RsGluR) encoding a glutamate receptor-like protein from small radish has been cloned. Transgenic Arabidopsis plants overexpressing the radish gene were developed (Kang et al. 2006). The transgenic plants showed increased Ca2+ influx in response to glutamate treatment. Overexpression of RsGluR resulted in upregulation of several Arabidopsis defensin genes encoding antifungal defensins. The transgenic plants showed increased resistance to the necrotrophic fungal pathogen Botrytis cinerea (Kang et al. 2006). These results suggest that genes encoding glutamate receptor-like channels can be bioengineered to activate Ca2+ signaling system for effective disease management.

2.4 Engineering H+ -ATPase for Plant Disease Management

29

2.4 Engineering H+ -ATPase for Plant Disease Management H+ -ATPase pump or proton pump plays important role in Ca2+ signaling system. The plasma membrane H+ -ATPase is an H+ pump. The plasma membrane H+ ATPases generate an H+ -gradient across the plant plasma membrane. The proton gradient also creates an electrical potential, which is used to drive cation uptake through ion channels (Palmgren 1998; Palmgren and Harper 1999; Elmore and Coaker 2011; Vidhyasekaran 2014, 2016). Activation or inhibition of the H+ -ATPase modulates membrane potential (Ward et al. 2009). Changes in membrane potential alter the activities of voltage-gated channels and control ion flux at the plasma membrane (Haruta et al. 2010; Elmore and Coaker 2011). Pathogen-associated molecular patterns (PAMPs) trigger either H+ -ATPase activation concomitant with extracellular acidification and membrane hyperpolarization, or H+ -ATPase inactivation resulting in the depolarization of the plasma membrane (Wevelsiep et al. 1993; VeraEstrella et al. 1994a; Hammond-Kosack et al. 1996; Xing et al. 1996). Depolarization/hyperpolarization of cell membrane may modulate Ca2+ influx in plant cells (White and Broadley 2003; Vidhyasekaran 2014, 2016). The activation of H+ -ATPase appears to be modulated by Ca2+ influx—induced calcium dependent protein kinase (CDPK) (Camoni et al. 1998b; Schaller and Oecking 1999; Vidhyasekaran 2014, 2016). The CDPK phosphorylates H+ -ATPase and the phosphorylation site is located at the C-terminal domain of H+ -ATPase (Camoni et al. 1998a). Phosphorylation of H+ -ATPase is stimulated by the addition of Ca2+ and by a decrease in pH, from 7.2 to 6.2, suggesting that changes in the cytoplasmic Ca2+ and pH are potentially important elements in modulating the kinase-mediated phosphorylation (Schaller and Sussman 1988). The H+ -ATPase might actually become activated following a dephosphorylation reaction preceeded by phosphorylation reaction by CDPK (Palmgren and Harper 1999). The elicitorinduced stimulation of the plasma membrane H+ -ATPase was inhibited by okadaic acid, a phosphatase inhibitor, but not by straurosporine, a protein kinase inhibitor in tomato, suggesting that protein dephosphorylation was required for increased H+ -ATPase activity (Vera-Estrella et al. 1994a). Plasma membrane H+ -ATPase play important role in plant innate immune responses (Vidhyasekaran 2014, 2016). Perception of flg22 by the PRR FLS2 results in rapid membrane depolarization and alkalinization of the apoplast, probably induced by inhibition of H+ -ATPases and activation of anion channels (Nühse et al. 2007; Jeworutzki et al. 2010; Keinath et al. 2010). PAMP-induced calcium influx at the plasma membrane has been shown to contribute to plasma membrane H+ -ATPase regulation in plant cells (Boller and Felix 2009; Kim et al. 2010; Vidhyasekaran 2014). Manipulation of the H+ -ATPase proton pump has been shown to be a potential tool for management of crop diseases. Transgenic tobacco plants expressing the bacterio-opsin proton pump derived from the bacterium Halobacterium halobium showed enhanced resistance against Pseudomonas syringae pv. tabaci (Fig. 2.4; Pontier et al. 2002) and also against Tobacco mosaic virus (Pontier et al. 2002).

30

2 Manipulation of Calcium Ion Influx …

Bacterial population (log cfu/Cm2)

9 8 7 6 5 4 3 2 1 0

Wild-type plants

Transgenic plants expressing bacterioopsin gene

Fig. 2.4 Transgenic tobacco plants expressing bacterio-opsin gene show enhanced resistance against Pseudomonas syringae pv. tabaci (Adapted from Pontier et al. 2002)

Transgenic potato plants expressing bacterio-opsin gene showed systemic acquired resistance (SAR) against the oomycete pathogen Phytophthora infestans (Abad et al. 1997). Expression of bacterio-opsin was found to lead to the insertion of a passive proton channel into the plasma membrane. This channel may translocate protons in a passive way that responds to the pH gradient across the plasma membrane maintained by the plasma membrane H+ -ATPase which pumps protons outward into the apoplast. The activity of this channel in the plasma membrane resulted in induction of hypersensitivity-associated responses including enhanced resistance against a broad spectrum of plant pathogens in tobacco (Pontier et al. 2002). These results suggest that some crop diseases can be managed by activating the H+ -ATPase pump.

2.5 Molecular Manipulation of H+ -ATPase Proton Pump by Laminarin for Crop Disease Management Laminarin is a linear β-1,3-glucan and several commercial formulations based on laminarin have been developed such as Vacciplant, Iodus40 and Physpe4 and these were derived from the brown alga Laminaria digitata (Aziz et al. 2003; RenardMerlier et al. 2007). Laminarin activates the plant innate immunity system in plants. The earliest event in the activation of immunity system is the induction of Ca2+ signaling system. Laminarin induced an increase in Ca2+ influx within a few minutes after treatment and the maximum influx was observed at 15 min in cultured grapevine cells (Aziz et al. 2003). Alkalinization of the incubation medium is an important event in elicitor-treated cell suspensions. Treatment of grapevine cells with laminarin caused an increase in the pH of the medium within 30 min (Aziz et al. 2003). Laminarin

2.5 Molecular Manipulation of H+ -ATPase Proton Pump …

31

treatment induced within a few minutes a 1.9-pH-units alkalinization of the extracellular medium when added to suspension-cultured tobacco cells (Klarzynski et al. 2000). The elicitors have been shown to trigger apoplastic alkalinization combined with cytosolic acidification in plant cells (Sakano 2001; Felle et al. 2004). Transient shifts of intracellular and apoplastic pH have been reported to be essential steps in several signal transduction processes (Felle et al. 2004). K+ /H+ exchange response is an important component in the apoplastic alkalinization (Orlandi et al. 1992; Felix and Boller 1995). The enzyme H+ /K+ -ATPase is a proton pump which is responsible for the apoplastic alkalinization and acidification of cytoplasm (Vidhyasekaran 2014). The enzyme is a member of the P-type ATPase superfamily, a large family of related proteins that transport ions across cell membranes. As an ion pump, the H+ /K+ -ATPase is able to transport ions against a concentration gradient using energy derived from the hydrolysis of ATP. The enzyme transports one H+ in exchange of one K+ (Kuhlbrandt 2004; Vidhyasekaran 2014). The K+ /H+ exchange response may be mediated by Ca2+ influx (Atkinson et al. 1990). The Ca2+ -dependent protein kinase, activated by increased cytosolic Ca2+ , may evoke ion fluxes that lead to extracellular alkalinization (Schaller and Oecking 1999). Laminarin triggers within moments of treatment, a transient production of H2 O2 in grapevine cells. The oxidative burst was observed within 10 min after laminarin application (Aziz et al. 2003). It is known that Ca2+ influx regulates NAD kinase, which generates NADPH for NADPH oxidase activity (Harding et al. 1997). Increase in NADPH oxidase activity results in generation of ROS (Desikan et al. 1998). Laminarin treatment induced accumulation of SA in treated tobacco cells (Klarzynski et al. 2000). Salicylate (SA) signaling system is an important downstream event of Ca2+ influx (Du et al. 2009; Boursiac et al. 2010; Chen et al. 2011; Wang et al. 2011; Truman and Glazebrook 2012; Wan et al. 2012; Vidhyasekaran 2015). Ca2+ influx plays an important role in triggering SA signaling system (Garcia-Brugger et al. 2006; Ahn et al. 2007). Laminarin induces expression of LOX gene encoding lipoxygenase in grapevine cells, which is a key enzyme in JA biosynthesis (Aziz et al. 2003; Balbi and Devoto 2008; Vidhyasekaran 2015). Calcium ion influx— induced H2 O2 production triggers increases in lipoxygenase activity (Zhao and Sakai 2003). Induction of lipoxygenase has also been reported in tobacco cells (Klarzynski et al. 2000). These results suggest that laminarin may induce defense responses by activating both SA and JA signaling systems. Laminarin induces several defense responses. It triggers the expression of several defense-related genes. It induces the expression of PAL (encoding a phenylalanine ammonia-lyase, which is a key enzyme in synthesis of phenolics) in grapevine cells (Aziz et al. 2003). Laminarin triggered strong induction of PAL and caffeic acid O-methyltransferase activities in tobacco cells (Klarzynski et al. 2000). Both the enzymes are key enzymes involved in lignin biosynthesis (Vidhyasekaran 2007). Laminarin induced several PR proteins in different plants. It enhanced the expression of GLU1 (encoding a basic β-1,3-glucanae [PR-2 protein]), CHIT1b, CHIT3 and CHIT4c (the three PR genes encoding chitinases [PR-3 proteins]), and PIN (encoding a serine-proteinase inhibitor; PR-6 protein) genes in grapevine cells (Aziz et al. 2003). Laminarin induced PR-1, PR-2, PR-3, and PR-5 proteins in tobacco plants

32

2 Manipulation of Calcium Ion Influx …

(Klarzynski et al. 2000). All these PR proteins are known to have antimicrobial action (Vidhyasekaran 2007). Laminarin induced STS1 (encoding a stilbene synthase involved in biosynthesis of phytoalexins) in grapevine cells (Aziz et al. 2003). Large amounts of the phytoalexins resveratrol and ε-viniferin were produced in grapevine cells in response to laminarin treatment (Aziz et al. 2003). These phytoalexins show antibiotic activities (Coutos-Thévenot et al. 2001). Commercial formulations of laminarin have been shown to control oomycete, fungal, and bacterial pathogens in monocot and dicot plants. Laminarin effectively controlled the grapevine downy mildew disease caused by the oomycete pathogen Plasmopara viticola (Fig. 2.5; Aziz et al. 2003). It also controlled the necrotrophic fungal pathogen Botrytis cinerea infection in grapevine (Aziz et al. 2003). Iodus 40 reduced powdery mildew (Blumeria graminis f. sp. tritici) incidence in wheat (Renard-Merlier et al. 2007). Physpe controlled fire blight of apple caused by Erwinia amylovora (Holtz et al. 2008). Vacciplant reduced the incidence of fire blight (E. amylovora) of pears (Adaskaveg et al. 2006). Laminarin could protect tobacco against E. carotovora infection (Klarzynski et al. 2000). These studies reveal the potential of laminarin in management of crop diseases and may be useful as a component in the integrated disease management strategy. Efficacy of laminarin improves when it is subjected to chemical sulfation (Ménard et al. 2004; Trouvelot et al. 2008). The sulfated laminarin elicits a wider range of defense responses than unsulfated laminarin. While laminarin controls oomycete, fungal, and bacterial diseases, it is ineffective in controlling virus diseases. In contrast, sulfated laminarin triggers resistance also against virus diseases. Sulfated laminarin controls Tobacco mosaic virus infection in tobacco (Ménard et al. 2004). Sulfated laminarin-induced JA signaling system pathway and callose deposition appear to contribute for the induced resistance to the downy mildew oomycete pathogen Plasmopara viticola in grapevine (Trouvelot et al. 2008). Sulfated laminarin can be developed as commercial product to manage wide range of pathogens. 30

Infected leaf surface (%)

25

20

15

10

5

0

Control

Laminarin treatment

Fig. 2.5 Effect of laminarin treatment on the development of downy mildew (Plasmopara viticola) on grapevine plants (Adapted from Aziz et al. 2003)

2.6 Manipulation of H+ -ATPase Using Chitosan Commercial Formulations

33

2.6 Manipulation of H+ -ATPase Using Chitosan Commercial Formulations Chitosan has been developed as a plant defense activator for management of crop diseases. It is a linear aminopolysaccharide of glucosamine and N-acetylglucosamine units and is obtained by alkaline deacetylation of chitin extracted from the exoskeleton of crustaceans such as shrimps and crabs (Badawy and Rabea 2011). Several commercial formulations, such as Elexa, Chitogel, Elexa 4 Plant Defense Booster and ChitaPlant, have been developed in USA, France, and Germany (Elmer and Reglinski 2006). Chitosan specifically modulates Ca2+ influx-mediated signaling systems (Zhao and Sakai 2003; Zuppini et al. 2004; Amborabé et al. 2008; Iriti and Faoro 2009). The cell death kinetic induced by chitosan was delayed by Verapamil, a calcium channel blocker, suggesting the importance of chitosan in Ca2+ signaling system (Iriti et al. 2006). Chitosan treatment inactivates H+ -ATPase resulting in membrane depolarization, which is involved in increasing Ca2+ influx (Amborabé et al. 2008; Vidhyasekaran 2014). Chitosan treatment induces several defense responses conferring resistance against a wide range of diseases (Table 2.1; Agrawal et al. 2002; Hu et al. 2004; Mandal and Mitra 2007; Faoro and Iriti 2007; Iriti and Faoro 2008; Hewajulige et al. 2009; Jayaraj et al. 2009; Rappussi et al. 2009). Chitosan has been found to be highly effective against oomycete (El Ghaouth et al. 1994; Sharathchandra et al. 2004; Aziz et al. 2006; Falcón et al. 2008; Manjunatha et al. 2008; Nandeeshkumar et al. 2008; Postma et al. 2009; Sunpapao and Ponsuriya 2014), fungal (Gorbatenko et al. 1996; Lafontaine and Benhamou 1996; Bell et al. 1998; Benhamou et al.1998; Reddy et al. 1999; Isebaert et al. 2002; Ait Barka et al. 2004; Liu et al. 2007; Prapagdee et al. 2007; Faoro et al. 2008; Jayaraj et al. 2009; Li et al. 2009; Moret et al. 2009; Rahman et al. 2009; Iriti et al. 2011; Dafermos et al. 2012; El-Mohamedy et al. 2014; Sathiyabama et al. 2014), bacterial (Algam et al. 2010), and viral (Iriti et al. 2006; Faoro and Iriti 2007; Zhao et al. 2007; Faoro et al. 2008; Hu et al. 2008, 2009; Iriti and Faoro 2008; Moret et al. 2009; El-Dougdoug and El-Shamy 2011; Mishra et al. 2014) diseases. Chitosan not only controls wide range of crop diseases, but also promotes crop growth (Kowlaski et al. 2006; Guan et al. 2009; Boonreung and Boonlertnirum 2013). It also increases crop yield (Boonlertnirun et al. 2008; Asghari-Zakaria et al. 2009).

2.7 Engineering Annexins for Crop Disease Management Annexins are Ca2+ -dependent phospholipid-binding proteins (Jami et al. 2012; Vidhyasekaran 2014, 2016). Annexins are membrane binding proteins that can form Ca2+ -permeable conductances in vitro (Laohavisit et al. 2012). Plant annexins are capable of mediating passive, channel-like Ca2+ transport (Mortimer et al. 2008; Laohavisit et al. 2009, 2010; Laohavisit and Davies 2011). A maize annexin preparation was found to promote Ca2+ influx into root epidermal protoplasts

34

2 Manipulation of Calcium Ion Influx …

Table 2.1 Management of crop diseases by manipulating plant immune responses using chitosan Plant

Disease

Pathogen

References

Wheat

Crown rot

Fusarium graminareum

Reddy et al. (1999)

Barley

Powdery mildew

Blumeria graminis

Faoro et al. (2008)

Rice

Dirty panicle disease

Helminthosporium oryzae, Curvularia lunata, Fusarium moniliforme

Boonreung and Boonlertnirum (2013)

Tomato

Crown and root rot

Fusarium oxysporum f. sp. radicis-lycopersici

Benhamou and Thériault (1992), Benhamou et al. (1994), Lafontaine and Benhamou (1996), Benhamou et al. (1998), El-Mohamedy et al. (2014)

Fusarium wilt

Fusarium oxysporum f. sp. lycopersici

Mandal and Mitra (2007)

Ralstonia wilt

Ralstonia solanacearum

Algam et al. (2010)

Powdery mildew

Oidium lycopersici

Isebaert et al. (2002), Gorbatenko et al. (1996)

Leveillula taurica

Dafermos et al. (2012)

Early blight

Alternaria solani

Jayaraj et al. (2009)

Tomato leaf curl

Tomato leaf curl virus

Mishra et al. (2014)

Gray mold

Botrytis cinerea

Liu et al. (2007)

Blue mold

Penicillium expansum

Liu et al. (2007)

Potato

Dry rot

Fusarium sulphureum

Li et al. (2009)

Cucumber

Powdery mildew

Sphaerotheca fuliginea

Moret et al. (2009)

Tobacco

Carrot Bean

Erysiphe cichoracearum

Moret et al. (2009)

Gray mold

Botrytis cinerea

Ben-Shalom et al. (2003)

Root rot

Pythium aphanidermatum

El Ghaouth et al. (1994), Postma et al. (2009)

Tobacco mosaic

Tobacco mosaic virus

Zhao et al. (2007), Hu et al. (2009)

Tobacco necrosis

Tobacco necrosis virus

Iriti et al. (2006), Faoro and Iriti (2007) Falcón et al. (2008)

Black shank

Phytophthora parasitica

Black rot

Alternaria radicina

Jayaraj et al. (2009)

Sclerotinia rot

Sclerotinia sclerotiorum

Molloy et al. (2004)

Tobacco necrosis virus

Tobacco necrosis virus

Zhao et al. (2007), Hu et al. (2009) (continued)

2.7 Engineering Annexins for Crop Disease Management

35

Table 2.1 (continued) Plant

Disease

Pathogen

References

Celery

Fusarium yellows

Fusarium oxysporum

Bell et al. (1998)

Soybean

Sudden death syndrome

Fusarium solani f. sp. glycines

Prapagdee et al. (2007)

Sunflower

Downy mildew

Plasmopara viticola

Nandeeshkumar et al. (2008)

Pearl millet

Downy mildew

Sclerospora graminicola

Sharathchandra et al. (2004), Manjunatha et al. (2008)

Grapevine

Downy mildew

Plasmopara viticola

Aziz et al. (2006)

Powdery mildew

Uncinula necator

Gorbatenko et al. (1996), Iriti et al. (2011)

Gray mold/bunch rot

Botrytis cinerea

Ait Barka et al. (2004), Elmer and Reglinski (2006)

Banana

Bunchy top

Banana bunchy top virus

El-Dougdoug and El-Shamy (2011)

Papaya

Anthracnose

Colletotrichum gloeosporioides

Rahman et al. (2009), Hewajulige et al. (2009)

Orange fruits

Black spot

Guignardia citricarpa

Rappussi et al. (2009)

(Laohavisit et al. 2009). It also formed a Ca2+ -permeable conductance in planar lipid bilayers that resembled plant plasma membrane Ca2+ -permeable nonselective cation channel (Laohavisit et al. 2009). Pepper annexin mediates Ca2+ influx into artificial vesicles (Hofmann et al. 2000). Laohavisit et al., (2010) reported that annexins form a passive Ca2+ transport pathway in maize. Arabidopsis loss-of-function mutant for annexin1 (Atann1) was found to lack epidermal Ca2+ conductance (Laohavisit et al. 2012). An ROS-activated Ca2+ conductance was reconstituted by recombinant annexin1 (ANN1) in planar lipid bilayers (Laohavisit et al. 2012). These results suggest that annexin is a novel Ca2+ -permeable transporter. A full-length cDNA for a gene encoding an annexin protein was isolated from Brassica juncea (AnnBj1) (Jami et al. 2008). Transgenic tobacco plants ectopically expressing AnnBj1 under the control of constitutive CaMV 35S promoter were developed. These transgenic plants showed enhanced expression of several pathogenesisrelated proteins and increased peroxidase activity. The transgenic tobacco plants expressing the annexin gene from B. juncea showed enhanced resistance to the oomycete pathogen Phytophthora parasitica var. nicotianae (Jami et al. 2008).

36

2 Manipulation of Calcium Ion Influx …

2.8 Bioengineering Calmodulin Genes to Promote Immune Responses for Plant Disease Management Calmodulin (CaM) is a Ca2+ sensor protein (Reddy et al. 2011; Vidhyasekaran 2014, 2016). Plants produce numerous calmodulin isoforms that exhibit differential gene expression patterns and sense different Ca2+ signals (Park et al. 2004). Several CaM genes have been isolated from plants (Heo et al. 1999; Park et al. 2004; Takabatake et al. 2007; Kim et al. 2009). CaM activates numerous proteins participating in immune signaling systems (Heo et al. 1999). Calmodulin isoforms transduce the defense signal and up-regulate the expression of several pathogenesis-related (PR) genes involved in conferring resistance against pathogens (Park et al. 2004). The tobacco CaM gene, NtCaM13, induces resistance against the bacterial pathogen Ralstonia solanacearum, the fungal pathogen Rhizoctonia solani, and the oomycete pathogen Pythium aphanidermatum in tobacco (Takabatake et al. 2007). The constitutive expression of the soybean CaM genes in transgenic tobacco plants constitutively expressed genes encoding PR-1a, PR-1b, PR2, PR3, PR4, PR5, class III acidic chitinase and class III basic chitinase (Heo et al. 1999). Gm-CaM-4 and -5 are two divergent calmodulin isoforms from the soybean (Glycine max) that have been reported to be involved in plant disease resistance. Transgenic Arabidopsis plants overexpressing the soybean GmCaM-4/GmCaM-5 genes showed increased constitutive PR gene expression and showed enhanced disease resistance. GmCaM-4/5appear to activate trans-acting elements that bind to cis-acting elements in the Arabidopsis PR-1 promoter (Park et al. 2004). These results suggest that calmodulin genes can be engineered to activate defense signaling systems for effective disease management. Transgenic tobacco plants constitutively expressing soybean CaM genes (SCAM4 or SCAM5) were developed. These transgenic plants showed resistance to the bacterial pathogen Pseudomonas syringae pv. tabaci (Fig. 2.6; Heo et al. 1999). When the 5 4.5

Bacteria (log cfu/ml)

4 3.5 3 2.5 2 1.5 1 0.5 0 Wild-type plants

Transgenic tobacco plants expressing soybean calmodulin gene

Fig. 2.6 Transgenic tobacco plants expressing soybean calmodulin gene show enhanced resistance to Pseudomonas syringae pv. tabaci (Adapted from Heo et al. 1999)

% infected cotyledons with heavy sporulaƟon of pathogen

2.8 Bioengineering Calmodulin Genes to Promote Immune …

37

60

50

40

30

20

10

0 Wild-type plants

Transgenic plants expressing CaCaM1 calmodulin gene

Fig. 2.7 Transgenic Arabidopsis plants overexpressing Capsicum annuum calmodulin 1 (CaCaM1) gene show enhanced resistance to Hyaloperonospora parasitica (Adapted from Choi et al. 2009)

tobacco plants were inoculated with the black shank oomycete pathogen Phytophthora parasitica pv, nicotianae, At 5 days after the pathogen inoculation, disease symptoms started to appear on the wild-type plants but not on the transgenic plants. By 7 days after inoculation, the wild-type plants had severe symptoms and eventually died by 8 days after inoculation. However, the inoculated transgenic plants remained healthy throughout the period (Heo et al. 1999). The transgenic plants also showed enhanced resistance against Tobacco mosaic virus (Heo et al. 1999). Transgenic overexpression of pepper calmodulin gene CaCaM1 activated ROS and NO generation and HR-like cell death conferring resistance to Xanthomonas campestris pv. vesicatoria in pepper leaves (Fig. 2.7; Choi et al. 2009). CaCaM1overexpressing Arabidopsis exhibited enhanced resistance to Pseudomonas syringae pv tomato DC3000 and Hyaloperonospora parasitica, which was accompanied by enhanced ROS and NO generation (Choi et al. 2009). However, these transgenic plants did not show resitance to the necrotrophic fungal pathogen Alternaria brassicicola. CaCaM1 expressing plants showed activation of SA-mediated signaling pathway, which is not sufficient to trigger resistance against necrotrophic pathogens (Choi et al. 2009). JA signaling system is involved in triggering resistance against necrotrophs (Thomma et al. 1998; Choi et al. 2009; Kidd et al. 2009; Méndez-Bravo et al. 2011; Moffat et al. 2012; Vidhyasekaran 2015). Treatment with the calcium channel blocker LaCl3 suppressed the ROS and NO bursts and HR-like cell death that were triggered by CaCaM1 expression in pepper and Arabidopsis (Choi et al. 2009). These results suggest that calcium influx is required for the activation of CaCaM1-mediated defense responses.

38

2 Manipulation of Calcium Ion Influx …

2.9 Engineering CBP60g Calmodulin-Binding Proteins for Disease Management CaM60s, a plant-specific family of CaM binding proteins have been detected in several plant species, including maize (Reddy et al. 1993), bean (Ali et al. 2003), tobacco (Lu and Harrington 1994), and Arabidopsis (Reddy et al. 2002; Wang et al. 2009; Zhang et al. 2010). Binding of CaM to CBP60g has been shown to be essential for the function of CBP60g (Wang et al. 2009). CBP60g is involved in activating SA biosynthesis (Wang et al. 2009; Zhang et al. 2010; Vidhyasekaran 2015). Arabidopsis CBP60g positively affects the expression of SID2, which encodes an isochorismate synthase (ICS) that is involved in biosynthesis of SA (Wang et al. 2011). CBP60g shows DNA binding activity, and it preferentially binds to a DNA sequence that contains AATTTT, which is present in the promoter of ICS1 (Wang et al. 2011). Transgenic Arabidopsis plants overexpressing CBP60g gene were developed and these transgenic plants showed enhanced resistance against the bacterial pathogen Pseudomonas syringae (Wan et al. 2012). Overexpression of CBP60g in Arabidopsis caused elevated SA accumulation and increased expression of the defense genes (Wan et al. 2012). The results suggest that engineering the calmodulin-binding protein gene may be a potential approach for developing disease-resistant plants.

2.10 Engineering Calcium-Dependent Protein Kinase Genes for Crop Disease Management Calcium-dependent protein kinases (CDPKs) are Ca2+ sensor proteins in transducing differential Ca2+ signatures activating complex downstream responses (Boudsocq et al. 2010; Gao et al. 2014; Vidhyasekaran 2014). CDPKs play versatile roles in the activation and repression of enzymes, channels, and transcription factors (Boudsocq and Sheen 2013). Several CDPKs have been reported in plants (Hrabak et al. 2003). Several CDPK genes have been detected in soybean, rice, tomato, maize, and Arabidopsis (Harmon et al. 2001). Individual isoforms of CDPKs may have different functions and participate in multiple distinct signaling pathways (Harmon et al. 2001; Ludwig et al. 2004). CDPKs target several proteins involved in immune signaling systems (Schaller and Oecking 1999; Xing et al. 2001; Sanders et al. 2002; Sebastiá et al. 2004; Mori et al. 2006; Kobayashi et al. 2007; Yu et al. 2007). The potential of developing disease resistant plants against wide range of pathogens using CDPK genes has been reported. Transgenic Arabidopsis plants overexpressing the CDPK gene, AtCPK1, were developed (Coca and Segundo 2010). These transgenic plants showed enhanced resistance to Fusarium oxysporum infection (Fig. 2.8; Coca and Segundo 2010). The transgenic plants also showed resistance against the necrotrophic fungal pathogen Botrytis cinerea and the bacterial pathogen Pseudomonas syringae (Coca and Segundo 2010). Over-expression of AtCPK1 resulted in accumulation of SA and constitutive expression of defense responses (Coca and Segundo 2010).

2.10 Engineering Calcium-Dependent Protein Kinase Genes …

39

35 30

% survival

25 20 15 10 5 0 Wild-type plants

Transgenic plants expressing CDPK gene

Fig. 2.8 Transgenic Arabidopsis plants expressing the calcium-dependent protein kinase gene, AtCPK1 show resistance to Fusarium oxysporum infection (Adapted from Coca and Segundo 2010)

Transgenic rice plants expressing the wheat calcium-dependent protein kinase gene TaCPK2-A were developed (Geng et al. 2013). These transgenic rice plants showed enhanced resistance against the bacterial blight pathogen X. oryzae pv. oryzae (Fig. 2.9; Geng et al. 2013). Overexpression of TaCPK2—A in a susceptible japonica rice cultivar induced resistance to the bacterial blight pathogen in both seedlings and booting stage plants. Populations of X. oryzae pv. oryzae in the TaCPK2-A transgenic plants were decreased more than 10-fold compared with the control plants (Geng et al. 2013). 45 40 35

Lesion area (%)

30 25 20 15 10 5 0 Control

Transgenic rice line expressing TaCPK2-A gene

Fig. 2.9 Transgenic rice plants expressing wheat calcium-dependent protein kinase gene TaCPK2-A show resistance against Xanthomonas oryzae pv. oryzae (Adapted from Geng et al. 2013)

40

2 Manipulation of Calcium Ion Influx …

2.11 Manipulation of Ca2+ -Dependent Signaling Pathway by Vitamin B1 Vitamin B1 (thiamine) is a B-complex vitamin and occurs in plants as free thiamine and the phosphorylated forms thiamine monophosphate (TMP), thiamine pyrophosphate (TPP), and thiamine triphosphate. Thiamine induces systemic acquired resistance (SAR). It activates SAR-related genes in rice, tobacco, tomsto, cucumber, and Arabidopsis (Ahn et al. 2005). Thiamine (50 mM) treatment induced resistance against the rice blast disease caused by Magnaporthe oryzae (Ahn et al. 2005). It also induced resistance to the rice bacterial blight pathogen X. oryzae pv. oryzae. Thiamine protected susceptible tobacco plants against infection by Pepper mild mottle virus (PMMoV ). Typical symptoms of systemic PMMoV infection appeared in leaves of untreated control plants, but no clear symptoms or visible disease progress were observed in thiamine-treated tobacco plants. Replication of PMMoV was almost completely inhibited in thiamine-treated leaves. Thiamine also induced resistance against the powdery mildew pathogen Spherotheca fuliginea and the anthracnose pathogen Colletotrichum lagenarium in cucumber (Ahn et al. 2005). Thiamine treatment induced resistance against the bacterial pathogen Pseudomonas syringae pv. tomato in Arabidopsis (Ahn et al. 2005). Thiamine treatment alone did not induce defense response in rice plants. However, when the plants were challenge-inoculated with the virulent pathogen, defense response was induced within 24 h after inoculation (Ahn et al. 2005). It suggests that thiamine is involved in priming of rice plants to induce disease resistance. Thiamine may induce defense gene expression by triggering Ca2+ -dependent signaling pathway. It was demonstrated by using the calcium ion inhibitor LaCl3 , which blocks plasma membrane calcium channels. Four hours after spraying of Arabidopsis plants with 50 mM thiamine, LaCl3 was infiltrated into the leaves. When the calcium channel blocker LaCl3 was infiltrated into Arabidopsis plants, thiamine treatment could not induce expression of defense genes (Ahn et al. 2005). The results suggest the involvement of Ca2+ influx in the early events in induction of defense responses in thiamine-treated plants. Thiamine primed the rice plants to induce resistance after inoculation with the pathogen. The thiamine-treated rice plants infected with the blast pathogen M. oryzae showed a 2-fold increase in Ca2+ -induced protein kinase C (PKC) activity, as compared to mock-treated plants. Certain rice PKCs share biochemical characteristics with animal PKCs (Ahn et al. 2005). Downstream of Ca2+ -influx, ROS signaling system is induced by thiamine treatment (Ahn et al. 2005). Thiamine also activated SA-dependent signaling pathway (Ahn et al. 2005). Thiamine provides long-lasting protection against pathogens. No phytotoxic symptoms are seen in thiamine-treated plants (Ahn et al. 2005). Thiamine does not induce defense responses constitutively but acts only by priming of defense responses. Hence thiamine may not intervene in the yield potential of plants. These observations suggest that thiamine appears to be a potential tool to manage crop diseases by intervening in pathogenesis of various types of pathogens.

References

41

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Chapter 3

Manipulation of Reactive Oxygen Species, Redox and Nitric Oxide Signaling Systems to Activate Plant Innate Immunity for Crop Disease Management Abstract Reactive oxygen species (ROS) signaling system involves complex redox processes that require participation by specific signal molecules, such as H2 O2 and nitric oxide (NO), and antioxidants, such as tocopherols and riboflavin. ROS signaling network plays a central role in launching the defense. ROS mediates a reiterative signal network underlying systemic induced resistance. ROS appears to interact with various defense signaling systems. ROS induces NO signaling system, salicylic acid (SA) signaling system, ethylene (ET)-mediated signaling system, and jasmonic acid (JA)-dependent signaling system. ROS activates the mitogen-activated protein kinase (MAPK) system. BTH (benzo[1,2,3]thiadiazole-7-carbothioc acid S-methyl ester) is the most successfully developed commercial compound to manipulate ROS signaling system for management of viral, bacterial, and phytoplasma diseases and parasitic plants, which are difficult to be controlled by traditional chemical control methods. BTH has been shown to induce several genes with potential roles in establishing reducing conditions following the oxidative burst induced by it. Thiol-based redox signaling has been suggested to contribute to the activation of a primed state in BTHtreated plants. BTH treatment, which induces redox conditions, activates NPR1 (for non-expresser of PR gene 1) and induces resistance against pathogens. It induced NPR1 mRNA accumulation by several-fold. NPR1 gene is a master regulator of the systemic acquired resistance (SAR) in plants. NPR1 enhances the binding of transcription factors to the promoters of pathogenesis-related (PR) defense genes for activation. Riboflavin is another compound which can be used to manipulate ROS and redox signaling system. It induces H2 O2 production. Riboflavin induces priming of defense responses and triggers systemic resistance against pathogens. Vitamin B1 (thiamine) treatment induces systemic acquired resistance in susceptible plants through priming. It is a potential tool to manage pathogens through its action on ROS signaling system. Menadione sodium sulphite (MSB) is a water-soluble addition compound of vitamin K3 . It is an effective ROS generator producing superoxide radicals (O2 − ) and H2 O2 . MSB treatment induces systemic resistance by activating redox signaling systems. Some herbicides have been shown to act as plant innate immunity system activators. The herbicide lactofen targets protoporphyrinogen oxidase, which in turn causes singlet oxygen generation. Singlet oxygen is involved

© Springer Nature B.V. 2020 P. Vidhyasekaran, Plant Innate Immunity Signals and Signaling Systems, Signaling and Communication in Plants, https://doi.org/10.1007/978-94-024-1940-5_3

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in triggering ROS-mediated signaling system. Lactofen application provides significant control of fungal and oomycete diseases. Trifluralin, a dinitroaniline herbicide, induces disease resistance against several pathogens by manipulating redox signaling system. Glufosinate ammonium is a nonselective herbicide. It activates ROS-dependent SA signaling system and induces resistance against pathogens. Milsana (Reynoutria sachalinensis formulation) activates ROS-mediated signaling system and is highly effective in controlling powdery mildew diseases in crop plants. β-Aminobutyric Acid (BABA) has been shown to induce disease resistance against various pathogens by triggering ROS production. BABA-induced resistance is mostly based on priming of defense responses rather than on the direct activation of these defense responses. BABA has been shown to prime RbohD gene, which encodes a NADPH oxidase potentially involved in ROS production. Potassium dihydrogen phosphate induces systemic resistance by inducing a rapid generation of superoxide and hydrogen peroxide. Potassium phosphonate triggers ROS signaling systemmediated plant defense responses by rapidly releasing superoxide around the point of infection. Oxycom is a commercially available chemical containing reactive oxygen species. It acts as a plant innate immunity activator. Applications of Oxycom triggers plant immune system downstream of ROS. Several bacterial and fungal biocontrol agents have been shown to induce systemic resistance (ISR) against several plant pathogens in various crop plants. Some of the rhizobacteria activate the plant innate immune system by triggering the ROS signaling system. Pseudomonas fluorescens WCS374 is a potential tool to trigger ROS signaling system and confer resistance against pathogens. Serratia plymuthica ICI270, primes leaves for enhanced attackerinduced accumulation of ROS. It induces accumulation of ROS in leaves and induces systemic resistance. Bacillus mycoides elicits ISR by triggering ROS production. Silicon is another potential tool to enhance defense responses by activating ROS signaling system. Silicon treatment significantly alters the activity of lipoxygenase (LOX), which catalyzes the direct oxygenation of polyunsaturated fatty acids and produces O2 − . Several silicon-based formulations are available for management of crop diseases. Cysteine-rich receptor-like kinases (CRKs) are connected to redox and ROS signaling. Transgenic plants overexpressing CRK genes show enhanced disease resistance by triggering enhanced ROS production. L-type lectin receptor kinases (LecRKs) have been exploited to develop transgenic disease-resistant plants. These transgenic plants show enhanced production of ROS and trigger defense responses against pathogens. Peroxidases in the cell wall can generate apoplastic H2 O2 at neutral to basic pH in the presence of reductants in plant cells. It is possible to generate transgenic plants overexpressing peroxidase gene to overproduce peroxidase resulting in enhanced ROS accumulation. These transgenic plants show enhanced disease resistance. Super oxide dismutase gene has been engineered to activate ROSmediated immune signaling for disease management. Fungal glucose oxidase gene has been engineered to develop disease-resistant plants. Expression of the fungal glucose oxidase gene leads to elevated production of H2 O2 in the transgenic plants resulting in increased resistance. Sodium nitroprusside (SNP) is a NO generator and it effectively controls diseases. NO signaling system can be manipulated by using antisense technology for plant disease management. GSNOR (S-nitroso glutathione

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reductase) has been exploited using antisense strategy to develop transgenic plants expressing resistance against oomycete and bacterial pathogens. NOS (nitric oxide synthase) has been used to develop transgenic plants. The mammalian NOS isolated from rat brain has been shown to be a potential tool to develop transgenic plants expressing resistance against a wide range of pathogens. Keywords BTH · Riboflavin · Thiamine · Herbicides · Milsana · BABA · Priming · Systemic acquired resistance · Induced systemic resistance · Antisense strategy · NOS · GSNOR · Transgenic plants

3.1 Complexity of ROS-Redox-NO Signaling System The rapid and transient production of reactive oxygen species (ROS), also called oxidative burst or respiratory burst, is one of the most rapid defense responses observed in plants (Yang et al. 1997; Grant and Loake 2000; Faize et al. 2004; Asada 2006; Sagi and Fluhr 2006; Choi et al. 2007; Asai and Yoshioka 2009; L’Haridon et al. 2011; Lehtonen et al. 2012; Vidhyasekaran 2007, 2014, 2015, 2016). Reactive oxygen species include hydrogen peroxide (H2 O2 ), superoxide (O2 − ), singlet oxygen (1 O2 ), and hydroxyl radical (OH· ) (Grant and Loake 2000; Pieterse and Van Loon 2004; Vidhyasekaran 2014). The ROS signaling system involves complex redox processes that require participation by specific signal molecules, such as H2 O2 and nitric oxide, and antioxidants, such as tocopherols and riboflavin (Dong and Beer 2000; Neill et al. 2002). ROS mediates a reiterative signal network underlying systemic induced resistance (Fig. 3.1; Lee and Hwang 2005). ROS appears to interact with various defense signaling systems and the ROS signaling network plays a central role in launching the defense response (Vandenabeele et al. 2003; Petrov and Van Breusegem 2012; Vidhyasekaran 2016). ROS induces nitric oxide (NO) signaling system, salicylic acid (SA) signaling system, ethylene (ET)-mediated signaling system, and jasmonic acid

ROS NO

ROS

NO biosynthesis

SA biosynthesis

Redox Signaling System

JA biosynthesis

ET biosynthesis

Fig. 3.1 Components in the complex ROS signaling system

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(JA)-dependent signaling system (Desikan et al. 2001; Vranová et al. 2002; Gupta and Luan 2003; Vandenabeele et al. 2003; Desikan et al. 2005; Fedoroff 2006; Hancock et al. 2006; Torres et al. 2006; Vidhyasekaran 2015, 2016). H2 O2 production has been shown to be required for NO synthesis (Bright et al. 2006). NO is often produced at the same time and in the same locations in plants as ROS (Neill et al. 2003). NO is known to modify the same type of proteins which are modified by H2 O2 (Lindermayr et al. 2005). ROS activates the mitogen-activated protein kinase (MAPK). The ROS-activated MAPK modulates NO biosynthesis (Wang et al. 2010). H2 O2 stimulates salicylic acid (SA) biosynthesis in plants (Fig. 3.2; León et al. 1995; Kauss and Jeblick 1995; Vidhyasekaran 2015). SA is synthesized from benzoic acid (BA) (Yalpani et al. 1993). H2 O2 causes an intracellular accumulation of BA. The conversion of BA to SA is catalyzed by benzoic acid 2-hydroxylase (BA2H), an inducible enzyme that is synthesized de novo in response to increased BA level (León et al. 1993). The catalase-mediated release of molecular oxygen from peroxide may lead to the activation of BA2H, resulting in enhanced accumulation of SA (León et al. 1995). ROS may also be involved in triggering ethylene signaling system (Fig. 3.3). S-adenosyl-l-methionine synthetase is the first enzyme in the ethylene biosynthesis pathway and 1-aminocyclopropane-1-carboxylate (ACC) oxidase is the final stage Catalase H2O2

H2O2 degradation Release of Molecular Oxygen

Benzoic acid

Molecular Oxygen

Benzoic acid 2-hydroxylase

Salicylic acid biosynthesis Fig. 3.2 ROS stimulates salicylic acid biosynthesis pathway (Adapted from Yalpani et al. 1993; León et al. 1995)

3.1 Complexity of ROS-Redox-NO Signaling System

L-Methionine

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ROS - NO

S-adenosyl-L-methionine synthetase

S-Adenosyl-L-methionine

ACC synthase

ACC

ACC oxidase

ROS

Ethylene Fig. 3.3 ROS stimulates ethylene biosynthesis (Adapted from Vandenabeele et al. 2003)

enzyme involved in conversion of ACC to ethylene (Vidhyasekaran 2015). Transcript tags coding for both the enzymes are up-regulated by H2 O2 (Vandenabeele et al. 2003). Ethylene receptor ETR1 (for ethylene response 1) functions as an ROS sensor (Desikan et al. 2005). ROS stimulates ethylene biosynthesis (Fig. 3.4). The genes encoding lipase, lipoxygenase, 12-oxophytodienoate reductase (12-OPDA reductase), and divinyl ether synthase are activated in leaves accumulating ROS (Vranová et al. 2002; Vandenabeele et al. 2003) and these enzymes are involved in JA biosynthesis (Vidhyasekaran 2015). The ROS signal functions are manifested as a consequence of their ability to act as mobile carriers of an unpaired electron (Forman et al. 2004). Redox signaling occurs when at least one step in a signaling event involves one of its components being specifically modified by a reactive oxygen species through a reaction that is chemically reversible under physiological conditions and/or enzymatically catalyzed

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Membrane lipids Phospholipase

Activation

ROS

α-Linolenic acid Lipoxygenase

ROS-NO Activation

13-HPOT Allene oxide synthase

NO Activation

12,13-Epoxy-octadecatrienoic acid

Allene oxide cyclase 12-oxo-phytodienoic acid (OPDA)

12-oxophytodienoate reductase ROS/NO

Jasmonic acid (JA) Fig. 3.4 ROS stimulates JA biosynthesis (Adapted from Westernack and Hause 2013)

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(Forman et al. 2004). Signaling through the redox active molecule H2 O2 is important in inducing plant defense responses (Desikan et al. 2005). NPR1, the transcriptional regulatory cofactor, is activated by redox signaling in plants and NPR1 is involved in triggering defense responses (Fedoroff 2006; Vidhyasekaran 2014, 2016).

3.2 Manipulation of ROS Signaling System Using Benzothiadiazole (BTH) for Crop Disease Management 3.2.1 BTH Triggers Oxidative Burst and Accumulation of ROS Through Phospholipid Signaling Acibenzolar-S-methyl (ASM) (benzo[1,2,3]thiadiazole-7-carbothioc acid S-methyl ester; BTH) is the most successfully developed commercial compound to manipulate ROS signaling system for management of viral, bacterial, and phytoplasma diseases and parasitic plants, which are difficult to be controlled by traditional chemical control methods. Acibenzolar-S-methyl (ASM) is a benzothiadiazole compound. Benzothiadiazole (BTH) is a synonym of ASM. It is marketed in Europe as BION and as ACTIGARD in U.S.A. (Walters et al. 2005; Mandal et al. 2008; Vidhyasekaran 2004). The early signaling event in BTH-treated plants is the oxidative burst. BTH induced oxidative burst within 3–4 h after treatment in rice suspension-cultured cells (Chen et al. 2006). Treatment of rice suspension cells with BTH resulted in a significant accumulation of superoxide anion and H2 O2 (Chen et al. 2006). BTH induced faster and stronger accumulation of ROS in barley leaves in response to infection by Blumeria graminis (Faoro et al. 2008). BTH triggered an early oxidative burst in French bean infected with the rust fungus Uromyces appendiculatus (Iriti and Faoro 2003). H2 O2 accumulates in sunflower roots treated with BTH (Sauerborn et al. 2002). BTH activates phospholipid signaling system, which is involved in production of ROS. BTH triggers 1-phosphatidylinositol-4-phosphate 5-kinase (PIP5K) encoding genes in papaya (Fig. 3.5; Qiu et al. 2004). PIP5K phosphorylates phosphatidylinositol 4 phosphate to produce phosphatidyl 4,5-bisphosphate (PIP2), the precursor of diacylglycerol (DAG) (Lanteri et al. 2008). Phospholipase C (PLC) is the key enzyme, which hydrolyzes PIP2 to generate DAG (Lanteri et al. 2008). BTH induced the phosphoinositide-specific phospholipase gene OsPI-PLC1 in rice (Chen et al. 2006). DAG is phosphorylated to phosphatidic acid (PA) through the action of DAG kinase (Lanteri et al. 2008). BTH induced the diacylglycerol kinase gene OsDAGK1 in rice (Chen et al. 2006). BTH activates PLC and DAG kinase in plants in response to pathogen infection (Chen et al. 2007). PA is produced by the action of DAG kinase and PA is known to trigger the oxidative burst (Sang et al. 2001; de Jong et al. 2004; Park et al. 2004). PA is involved in the activation of NADPH oxidase and ROS is generated through

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Inositol lipids

Phosphoinositide-3-kinase

Phosphatidylinositol (PI) BTH

Phosphatidylinositol-4-phosphate (PIP)

1-Phosphatidylinositol-4-phosphate kinase (PIP5K)

Phosphatidylinositol-4,5-bisphosphate (PIP2) BTH Phospholipase C

BTH Diacylglycerol (DAG)

DAG kinase

Phosphatidic acid (PA)

NADPH oxidase

DAG kinase gene

Superoxide anion, H2O2

Fig. 3.5 BTH triggers accumulation of ROS through phospholipid signaling (Adapted from Qiu et al. 2004; Chen et al. 2006, 2007; Lanteri et al. 2008)

3.2 Manipulation of ROS Signaling System Using …

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the action of NADPH oxidase (Laxalt et al. 2007). PA and DAG directly activate NADPH oxidase by interacting with enzyme components (Palicz et al. 2001). PA has been shown to induce ROS in tomato cells (Laxalt et al. 2007). PA promotes superoxide-generating activity in plants through the activation of NADPH oxidase (Sang et al. 2001).

3.2.2 BTH Triggers Accumulation of ROS Through Action of Peroxidases and Superoxide Dismutases NADPH oxidases, which are inhibited by diphenyleneiodonium (DPI) but not by cyanide or azide, and cell wall peroxidases (Grant et al. 2000; Bolwell et al. 2002; Kadota et al. 2014), are the two important groups of enzymes involved in ROS production (Vidhyasekaran 2014). In rose cells H2 O2 is produced by a plasma membrane NADPH oxidase, whereas in bean cells H2 O2 is derived directly from cell wall peroxidases (Bolwell et al. 1998). The peroxidase activity rapidly increased in the pathogen-inoculated Japanese pear leaves pretreated with BTH. The peroxidase is known to be involved in the generation of ROS (Halliwell 1978; Bolwell et al. 1998). BTH activated superoxide dismutase (SOD) in Japanese pear plants upon challenge inoculation with the pathogen Venturia nashicola (Faize et al. 2004). BTH increases the expression of the H2 O2 forming enzyme SOD in cucumber after attack by the fungal pathogen Colletotrichum orbiculare (Deepak et al. 2006). The gene encoding SOD is also activated by BTH treatment in cucumber (Deepak et al. 2006). SOD is known to rapidly dismutate superoxide to form H2 O2 , which is the major ROS involved in defense responses (Grant and Loake 2000). These studies suggest that activation of peroxidase and SOD may result in accumulation of ROS and BTH treatment activates both the enzymes.

3.2.3 BTH May Trigger Accumulation of ROS Through Suppression of ROS-Degrading Enzymes Suppression of ROS-degrading enzymes may also result in accumulation of ROS in plants. BTH treatment suppressed ascorbate peroxidase gene (APX) expression in oilseed rape inoculated with the fungal pathogen Leptosphaeria maculans. The measured expression levels of the gene were comparable to those in non-inoculated control plants (Borges et al. 2003). BTH has been shown to inhibit ascorbate peroxidase, increasing H2 O2 level in treated tobacco leaves (Wendehenne et al. 1998). It has been suggested that ascorbate peroxidase may play a role in the H2 O2 degrading pathway. Blocking the action of ascorbate peroxidase in the H2 O2 degrading pathway may lead to elevated levels of endogenous H2 O2 , which in turn, would contribute to

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defense gene expression (Borges et al. 2003). Catalase is another ROS-scavenging enzyme detected in plants. BTH inhibits catalase and increases H2 O2 level in BTHtreated tobacco leaves (Wendehenne et al. 1998). Peroxidase also reduces the activity of catalase and hence increases the production of H2 O2 (Milosevic and Slusarenko 1996).

3.2.4 Fine-Tuning of Accumulation of ROS by BTH BTH induces accumulation of ROS through different signaling pathways depending on the plant-pathogen interactions (Wendehenne et al. 1998; Orober et al. 2002; Borges et al. 2003; Faize et al. 2004; Cavalcanti et al. 2006; Deepak et al. 2006; Chen et al. 2007). The induced ROS triggers several downstream events inducing expression of several defense genes (Faize et al. 2004; Deepak et al. 2006; Faoro et al. 2008; Schreiber and Desveaux 2008), However, high accumulation of ROS is harmful to plant cells, resulting in necrosis (Manning et al. 2009). ROS species such as O2 − , OH· , and H2 O2 are strong oxidizing species that can rapidly attack all types of bio-molecules and damage the plant cells. For effective signal transduction, the accumulated ROS species have to be regulated so that the cells should not die and they should be active for triggering defense responses. For the protection from oxidative damage, plant cells contain both oxygen radical detoxifying enzymes such as catalase (CAT), peroxidase (POX) and superoxide dismutase (SOD), and antioxidant enzymes such as ascorbate peroxidase (APX) and glutathione-S-transferase (GST) (Alscher et al. 1997). These enzymes play a crucial role in the protection of the plant cell from oxidative damage at the sites of enhanced ROS generation (Ku´zniak and Sklodowska 2001). Thus for effective functioning of ROS signaling system in inducing defense responses, the ROS should be produced to a desirable level triggering defense responses, without causing cell damage. This can be achieved only by activating enzymes involved in both production and scavenging of ROS. Activation of ROS-scavenging systems may contribute to fine-tuning of ROS levels and their signaling properties in plant cells (Torres et al. 2006). BTH treatment fine-tunes ROS accumulation by scavenging excess ROS (Faize et al. 2004; Cavalcanti et al. 2006). The enzymes involved in scavenging of ROS such as catalase and ascorbate peroxidase were highly enhanced in BTH-pretreated Japanese pear plants upon challenge inoculation with Venturia nashicola (Faize et al. 2004). Catalase activity increased in BTH-treated apple leaves (Sklodowska et al. 2010). The genes involved in the production (SOD) and scavenging (catalase, CAT ) of ROS processes were involved in systemic resistance induced by BTH in cucumber (Deepak et al. 2006). Proteomic studies on proteins induced in cucumber leaves pretreated with BTH and challengeinoculated with Colletotrichum orbiculare revealed increased expression of pyridoxine biosynthesis protein, carbonic anhydrase, proteasome subunit (β1 type 1), phosphomannomutase, and ascorbate oxidase proteins. All the above proteins are well known to play a major role in scavenging of ROS (Deepak et al. 2008). Pyridoxine is known to inhibit superoxide radicals (Jain and Lim 2001). BTH treatment-induced

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carbonic anhydrase in cucumber is involved in scavenging of H2 O2 (Räisänen et al. 1999). The tobacco SA-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which shows antioxidant activity (Slaymaker et al. 2002). The proteasome comprising β1 subunit is a negative regulator of NADPH oxidase, a key enzyme involved in the generation of ROS (Lequeu et al. 2005). The phosphomannomutase is involved in biosynthesis of ascorbic acid, which is the substrate for the ROS scavenging enzyme ascorbate peroxidase (Qian et al. 2007). Ascorbate peroxidase is one of the major H2 O2 degrading enzyme (Qian et al. 2007). These observations suggest that BTH activates ROS signaling by fine-tuning of accumulation of ROS in plant cells. BTH treatment led to enhanced activities of antioxidant enzymes SOD and GST in tomato leaves. Increase in activities of the antioxidant enzymes due to BTH treatment resulted in reduction in the severity of the bacterial canker caused by Clavibacter michiganensis subsp. michiganensis in tomato (Soylu et al. 2003). It has been reported that ROS has a negative role in resistance or has a positive role in expansion of disease lesions during Botrytis cinerea–Nicotiana benthamiana interaction (Asai and Yoshioka 2009). In such interactions, enhanced activities of ROS scavenging enzymes would contribute for disease resistance. These studies suggest that the scavenging of ROS induced by BTH is involved in inducing resistance against pathogens. It has been suggested that scavenging of ROS would reduce the damage caused to the foliage by overproduction of ROS and help the plants remain healthy (Cavalcanti et al. 2006). BTH treatment-induced systemic resistance does not involve plant cell death, unlike pathogen induced systemic resistance. Collectively these results suggest that production and scavenging of ROS are one of the major events that occur during BTH-induced systemic resistance.

3.2.5 BTH Activates NPR1 by Inducing ROS-Mediated Redox Signaling BTH has been shown to induce several genes with potential roles in establishing reducing conditions following the oxidative burst induced by it (Qiu et al. 2004). BTH treatment induced two peroxidases and a cytochrome P450 that have likely roles in detoxifying ROS and establishing reducing conditions in the cell (Qiu et al. 2004). The genes encoding 2-oxoglutarate-dependent oxygenase (2OG-Fe(II) oxygenase), malate oxidoreductase, and hydroxyphenylpyruvate dioxygenase were induced by BTH treatment in papaya. These enzymes play an important role in inducing reducing conditions (Qiu et al. 2004). Thiol-based redox signaling has been suggested to contribute to the activation of a primed state in BTH-treated cucumber plants (Ku´zniak et al. 2014). BTH treatment, which induces redox conditions, activates NPR1 (for nonexpresser of PR gene 1) and induces resistance against pathogens. It induced NPR1

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mRNA accumulation by several-fold in rice (Chern et al. 2001). Increase in expression of NPR1 gene has been reported in papaya due to BTH treatment (Zhu et al. 2003). NPR1 gene is a master regulator of the systemic acquired resistance (SAR) in plants (Chern et al. 2008). NPR1 is an important regulator of defense responses downstream of SA (Mou et al. 2003; Zhang et al. 2003a, b; Mukherjee et al. 2010). It functions as a transcriptional co-activator of defense genes (Rochon et al. 2006). It contains a bipartite nuclear localization sequence and two potential protein-protein interaction domains (Cao et al. 1997; Ryals et al. 1996). Nuclear localization of NPR1 protein is essential for its function (Kinkema et al. 2000; Meur et al. 2006). Without induction, NPR1 protein forms an oligomer and is excluded from the nucleus. ROS-induced redox changes cause monomeric NPR1 to emerge and accumulate in the nucleus and activate transcription of defense genes (Kinkema et al. 2000; Mou et al. 2003). NPR1 enhances the binding of transcription factors to the promoters of pathogenesis-related (PR) defense genes for activation (Johnson et al. 2008). A canonical DNA-binding domain is absent in NPR1. It regulates PR gene expression only as a co-factor of the transcription factors, which interact with NPR1 (Chern et al. 2001; Fan and Dong 2002; Kesarwani et al. 2007). These studies suggest that BTH may activate the plant immune system by triggering accumulation of ROS, which may enhance the expression of NPR1, the key regulator of the long-lasting broadspectrum defense responses. Over-expression of NPR1 gene in transgenic plants has been widely reported to confer enhanced resistance to several pathogens (Cao et al. 1998; Chern et al. 2001; Friedrich et al. 2001; Makandar et al. 2006).

3.2.6 BTH Primes the Plants for Faster and Stronger Production of ROS When a treatment puts a plant in a state of increased alertness with no or only minimal gene induction it is called “priming” (Conrath et al. 2001, 2002, 2006; Conrath 2009; Kohler et al. 2002; Camañes et al. 2012; Slaughter et al. 2012; Vidhyasekaran 2016). The priming results in a faster and stronger induction of defense mechanisms after pathogen attack (Conrath 2011). BTH does not immediately induce ROS production, but conditions the plants for a faster and stronger response upon infection by pathogens (Faoro et al. 2008). BTH did not immediately induce ROS production, but primed the barley plants upon infection with the powdery mildew fungus Blumeria graminis (Faoro et al. 2008). This “primed” response included a more intense HR-associated oxidative burst and more extensive formation of cell wall appositions coupled with greater accumulation of phenolic compounds at sites of attempted fungal penetration (Faoro et al. 2008). Pretreatment of tomato plants with BTH before pathogen challenge reduced Botrytis cinerea infection development. Limited infection development was correlated with increasing generation of reactive oxygen species (H2 O2 and O2 − ) as well as increased peroxidase activity. H2 O2 and

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O2 − generation was weakly enhanced with BTH treatment alone or pathogen inoculation alone. In contrast, both the reactive oxygen species were highly enhanced in BTH pretreated plants upon challenge inoculation shortly after challenge. Collectively these results suggest the occurrence of priming during the tomato-BTH-and B. cinerea interaction (Malolepsza 2006). BTH changed the redox state of ascorbate, cysteine and glutathione pools, and induced accumulation of cysteine and glutathione bound to proteins. It also provoked profound accumulation of free salicylic acid and its glucosylated conjugates (Ku´zniak et al. 2014). Salicylic acid coupled with the ascorbate- and thiol-based redox signaling would have contributed to the BTHinduced priming in cucumber infected with Pseudomonas syringae pv. lachrymans (Ku´zniak et al. 2014).

3.2.7 Manipulation of Peroxidases by BTH for Crop Disease Management Plant peroxidases belong to a large multigene family. They belong to class I and class III peroxidases. The class I peroxidases include ascorbate peroxidases, which are involved in redox signaling. The class III peroxidases are involved in a broad range of defense processes and they are of glycoprotein in nature (Almagro et al. 2009). BTH treatment induces activities of peroxidases in several plants. BTH induced significant increases in peroxidase activities and conferred resistance against the bacterial blight caused by Xanthomonas axonopodis pv. malvacearum in cotton (Ishida et al. 2008). BTH significantly increased peroxidase activity in tomato plants (Cavalcanti et al. 2006, 2007). Peroxidase activity was approximately three times higher in tomato leaves treated with BTH than in untreated control plants and induced resistance against Clavibacter michiganensis subsp. michiganensis (Baysal et al. 2003). Early and enhanced expression of peroxidase activity seems to be an important element of induced resistance against Botrytis cinerea in tomato (Malolepsza 2006). In Festuca arundinacea, the highest peroxidase activity was detected 5 days after application of BTH (Kilic-Ekici and Yuen 2004). BTH induced systemic resistance in the susceptible wheat to the powdery mildew pathogen Blumeria graminis f. sp. tritici and it was accompanied by higher increase in peroxidase enzyme activity (Stadnik and Buchenauer 2000). BTH induced peroxidase activity in cocoa seedlings and it was correlated with induced resistance against Verticillium dahliae (Resende et al. 2002). BTH induced resistance against Fusarium and pink rots in harvested muskmelon. The protection effect of BTH was associated with the activation of peroxidase in treated muskmelons (Ge et al. 2008). Postharvest BTH treatment induced peroxidase activity in Hami melons and reduced decay severity caused by Alternaria alternata, Fusarium semitectum and Trichothecium roseum (Bi et al. 2006). BTH may induce peroxidase activity in plants, mostly when the plants were challenged with pathogens. Peroxidase was weakly activated when BTH alone or pathogen inoculation alone and highly enhanced in BTH-pretreated plants upon

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Peroxidase activity (nmol/min/mg protein)

300 250 200 150 100 50 0 BTH+pathogen

Water+Pathogen

BTH alone

Water alone

Fig. 3.6 Priming of peroxidase activity by BTH in Japanese pear leaves inoculated with Venturia nashicola (Adapted from Faize et al. 2004)

challenge inoculation with the pathogen Venturia nashicola in Japanese pear leaves, suggesting the occurrence of priming phenomenon in induction of peroxidase activity in plants (Fig. 3.6; Faize et al. 2004). Basil (Ocimum basilicum) plants treated with BTH and challenged with the oomycete pathogen Peronospora belbahrii showed significantly higher peroxidase activity than the untreated control (Mersha et al. 2013). BTH treatment triggered expression of the gene encoding lignin peroxidase (LPO) in cucumber after attack by the pathogen Colletotrichum orbiculare (Deepak et al. 2006). Cools and Ishii (2002) showed that peroxidase activity was directly induced by BTH in cucumber but its expression was further enhanced upon elicitation with the fungal pathogen C. orbiculare. Application of BTH induced a progressive and significant increase of peroxidase in locally treated tissues in tomato plants (Soylu et al. 2003). Such responses were expressed earlier and with a much higher magnitude when BTH-treated seedlings were challenged with the bacterial pathogen C. michiganensis. It suggests that a signal produced by the pathogen is essential for triggering enhanced synthesis and accumulation of peroxidase enzyme (Soylu et al. 2003). Peroxidases are involved in biosynthesis of lignins. Lignins are complex, cell wall phenolic heteropolymers. Hydroxycinnamyl alcohols (monolignols) are synthesized through phenylpropanoid pathway and the monolignols are converted into the lignin polymers through the action of peroxidases. Peroxidases provide the radicalgenerating capability for coupling each phenolic monomer into the complex lignin polymer (Fig. 3.7; Ralph et al. 2004). BTH treatment induces increased lignification and the increased deposition of lignin on plant cell walls fortifies the cell walls against the development of fungal pathogens. BTH treatment induced lignin peroxidase (LPO) gene in cucumber within 24 h after inoculation of the fungal pathogen Colletotrichum orbiculare (Deepak et al. 2006). The early expression of LPO gene coincided with subsequent deposition of

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MONOLIGNOLS

Coniferyl alcohol

Coumaryl alcohol

Sinapyl alcohol

Peroxidases

BTH

Lignin biosynthesis Fig. 3.7 Role of BTH-induced peroxidases in biosynthesis of lignins (Adapted from Ralph et al. 2004)

lignin in cucumber cell walls (Deepak et al. 2006). BTH treatment induced increases in lignin content in cocoa leaves and the increases were still higher in BTH pre-treated leaves challenge-inoculated with Verticillium dahliae (Cavalcanti et al. 2008). Peroxidases are associated with suberization (Passardi et al. 2004; Vidhyasekaran 2007). Suberin is a lipophilic extracellular barrier deposited on the inner side of the primary cell wall, providing a barrier to pathogen development conferring resistance against pathogens (Vidhyasekaran 2007). Peroxidases can create a physical barrier to limit pathogen invasion in host tissues by catalyzing the cross-linking of cell wall components. It interacts with extensins and wall-bound phenolics making the cell wall harder to penetrate (Passardi et al. 2004; Almagro et al. 2009).

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3.2.8 BTH Induces Several Host Plant Defense Responses Downstream of ROS Signaling 3.2.8.1

BTH Induces Increased Phenolic Biosynthesis

BTH is a host plant defense inducer, which induces systemic resistance against various pathogens, including fungi, bacteria, and viruses (Lawton et al. 1996; Tally et al. 1999; Oostendorp et al. 2001). BTH has been shown to induce defense mechanisms in apple (Thomson et al. 1999a, b), pear (Sobiczewski et al. 2001), strawberry (Terry and Joyce 2000), mango (Boshoff et al. 1998), rice (Schaffrath et al. 1997), wheat (Gorlach et al. 1996; Stadnik and Buchenauer 2000; Ge et al. 2001), barley (Besser et al. 2000), maize (Morris et al. 1998), tomato (Abbasi et al. 2001), bean (Bigirimana and Höfte 2002), cucumber (Benhamou and Bélanger 1998), cauliflower (Ziadi et al. 2001a), oilseed rape (Jensen et al. 1998), sunflower (Tosi and Zazzerini 2000; Prats et al. 2002), beet (Mouhanna 2000), spinach (Leskovar and Kolenda 2002), lettuce (Bertona et al. 2000), pepper (Buonaurio et al. 2002), cotton (Colson-Hanks and Deverall 2000), sugarcane (Ramesh Sundar et al. 2001), tobacco (Friedrich et al. 1996), and Arabidopsis (Fitzgerald et al. 2004). Increased phenolic contents were observed in various plants due to application of BTH (Ramesh Sundar et al. 2001; Suo and Leung 2002). Foliar application of BTH enhanced the levels of several phenolic compounds in strawberry (Karjalainen et al. 2002). Notable increases were detected in the levels of ellagi-tannin, ellagic acid and gallic acid derivatives, quercetin and kaempferol conjugates, catechin (+/−) and chlorogenic acid in strawberry treated with BTH (Karjalainen et al. 2002). Increased activities of several defense-related enzymes, such as phenylalanine ammonia-lyase (PAL), cinnamyl alcohol dehydrogenase (CAD), and peroxidase have been reported in BTH-treated plants (Burketová et al. 2000; Ge et al. 2001; Ramesh Sundar et al. 2001; Cools and Ishii 2002). PAL mRNA was strongly and persistently transcripted in BTH-treated bean plants since the sixth hour after treatment (Maffi et al. 2011). Inhibition of PAL by aminooxy-β-phenylpropionic acid (AOPP) suppressed the resistance induced by BTH in wheat plants against the powdery mildew pathogen Blumeria graminis (Stadnik and Buchenauer 2000). The results suggest that enhanced activity of PAL is the key component in BTH-induced activation of plant immune responses in wheat plants.

3.2.8.2

BTH Treatment Strengthens Cell Wall Barrier

ROS signaling system is involved in activation of various enzymes involved in plant cell wall thickening (Brisson et al. 1994; Otte and Barz 1996; Lamb and Dixon 1997; Vidhyasekaran 2007). BTH treatment induced strengthening of cell wall barrier and prevented spread of pathogens in epidermal layer and in the middle lamellae (Jiang et al. 2008). BTH treatment triggered more extensive formation of cell wall appositions at sites of attempted fungal penetration in barley leaves inoculated with

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Blumeria graminis (Faoro et al. 2008). BTH treatment induced callose synthase (CALS) gene in cucumber after attack by Colletotrichum orbiculare (Deepak et al. 2006). The early gene expression of CALS coincided with subsequent deposition of callose in cucumber cell walls (Deepak et al. 2006).

3.2.8.3

BTH Induces Biosynthesis of Phytoalexins

BTH treatment induces the expression of key enzymes involved in biosynthesis of phytoalexins in several plants (Latunde-Dada and Lucas 2001; Sauerborn et al. 2002; Osswald et al. 2004). Cowpea seedlings raised from BTH-treated seeds showed resistance to the anthracnose pathogen Colletotrichum destructivum. The resistance of BTH-treated tissues was associated with rapid transient increases in the activities of the key enzymes in the synthesis of phytoalexins, phenylalanine ammonialyase (PAL), and chalcone isomerase (CHI) (Latunde-Dada and Lucas 2001). Subsequently, there was an early, accelerated accumulation of the isoflavonoid phytoalexins kievitone and phaseollidin (Latunde-Dada and Lucas 2001). BTH induced synthesis of the phytoalexin apigenidin in sorghum mesocotyls (Osswald et al. 2004). BTH induced accumulation of the phytoalexin scopoletin in sunflower roots (Sauerborn et al. 2002).

3.2.8.4

Induction of PR Proteins by BTH

BTH treatment induces expression of several PR genes encoding various PR proteins belonging to different families, downstream of ROS-mediated SA signaling pathway regulated by NPR1. Accumulation of pathogenesis-related (PR-) proteins is commonly observed in plants treated with BTH (Ramesh Sundar et al. 2001; Ziadi et al. 2001a, b; Suo and Leung 2002). BTH treatment induces the expression of PR1 genes in various plant-pathogen interactions (Faize et al. 2004; Ahn et al. 2005; Medeiros et al. 2009). BTH induced expression of pr1 gene encoding PR-1 protein in Japanese pear leaves inoculated with Venturia nashicola (Faize et al. 2004). BTH treatment induced accumulation of PR-1 protein in rose plants inoculated with the black spot pathogen Diplocarpon rosae (Suo and Leung 2002). BTH induced accumulation of PR-1 protein in rice plants inoculated with the blast pathogen Magnaporthe oryzae (Ahn et al. 2005). BTH treatment increased accumulation of a PR1 mRNA and induced resistance against Phytophthora palmivora in papaya (Zhu et al. 2003). Induction of PR-1a gene expression by BTH treatment was observed in cucumber plants inoculated with Colletotrichum orbiculare (Cools and Ishii 2002). Although BTH invariably increases PR-1 expression in many plant-pathogen interactions, there are also reports that BTH does not induce accumulation of PR proteins in some of these interactions. BTH had no effects on the levels of PR-1 in cauliflower seedlings infected with Peronospora parasitica (Ziadi et al. 2001a). PR-1 protein may be involved in plant cell wall thickening and may offer resistance to the spread of pathogens in the apoplast (Benhamou et al. 1991). Santén et al. (2005) reported

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that PR-1 protein accumulated in mesophyll cell walls in barley leaves infected by Bipolaris sorokiniana. PR-1 protein was also detected on the host cell wall appositions. These observations suggest that PR-1 protein may have a role in strengthening host cell walls to prevent spread of the pathogens in host tissues. BTH also induced PR-2 protein in many plant-pathogen interactions (Ziadi et al. 2001a; Suo and Leung 2002; Bokshi et al. 2003). BTH triggered the induction and accumulation of PR-2 proteins in rose plants inoculated with Diplocarpon rosae (Suo and Leung 2002) and in cauliflower seedlings infected with the downy mildew pathogen Peronospora parasitica (Ziadi et al. 2001a). Accumulation of PR-2 protein was observed in sugarcane plants treated with BTH (Ramesh Sundar et al. 2001). PR-2 proteins show β-1,3-glucanase activity (Vidhyasekaran 2007). β-1,3glucanases (glucan endo-1,3-β-glucosidases) catalyze endo-type hydrolytic cleavage of the 1,3-β-D-glucosidic linkages in β-1,3-glucan. The bulk material of the cell wall of fungi and oomycetes is usually in the form of β-1,3-glucan (Duran and Nombela 2004). Bacterial cell wall also contains glucan (peptidoglycan). β-1,3-glucanases are hydrolytic enzymes capable of causing lysis of cell walls (Vidhyasekaran 2007). BTH treatment induced significant increases in β-1,3-glucanase activity in tea leaves challenged with the blister blight pathogen Exobasidium vexans (Ajay and Baby 2010). When BTH was sprayed on potato leaves, increases in β-1,3-glucanase activity were observed in leaves, stems, stolons, and tubers of the treated plants, suggesting that BTH induces systemic resistance in potato (Bokshi et al. 2003). Increased enzyme activity was recorded up to 45 days post-treatment (Bokshi et al. 2003). BTH treatment induced increases in activity of β-1,3-glucanase in sugar beet leaves inoculated with Cercospora beticola (Bargabus et al. 2002) and in papaya inoculated with Phytophthora palmivora (Zhu et al. 2003). BTH treatment induced three acidic β-1,3-glucanases and a basic β-1,3-glucanase in sugarbeet (Burketová et al. 1999). BTH induces collapse of hyphae of pathogens and the collapse of hyphae is accompanied by destruction of the fungal cell wall (Jiang et al. 2008). The fungal cell wall would have been degraded by the increased expression of the lytic enzyme β-1,3-glucanase. BTH induces various types of chitinases in plants challenge-inoculated with pathogens. Chitinases are endo β-1,4-glucosaminadases, which hydrolyze the βglycosidic bond at the reducing end of glucosaminides, which can be parts of various polymers, such as chitin, chitosan, or peptidoglycan found in various fungi and bacteria (Neuhaus 1999). BTH triggered the enhanced activation of chitinase (chi) gene expression in Japanese pear leaves infected by Venturia nashicola (Faize et al. 2004). BTH rapidly induced chitinase activities in Colletotrichum destructivum-infected cowpea seedlings (Latunde-Dada and Lucas 2001) and in Phytophthora palmivorainfected papaya (Zhu et al. 2003). BTH treatment rapidly induced chitinase activity in sugarcane plants (Ramesh Sundar et al. 2001). BTH treatment induced a 35-kDa chitinase in rice plants (Babu et al. 2003b). Resistance induced by BTH in cucumber against the scab pathogen Cladosporium cucumerinum was related to the rapid accumulation of chitinase (Narusaka et al. 1999).

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Several classes of chitinases have been detected in plants and four families of PR proteins (PR-3, PR-4, PR-8, and PR-11) show chitinase activity (Vidhyasekaran 2007). The PR-3 protein (chitinase) was invariably detected in BTH-treated plants (Mouhanna 2000; Ramesh Sundar et al. 2001; Bargabus et al. 2002; Suo and Leung 2002). Accumulation of PR-3 protein was observed in sugarcane plants treated with BTH (Ramesh Sundar et al. 2001). Pretreatment of BTH induced PR-3 proteins in rose plants infected by Diplocarpon rosae (Suo and Leung 2002) and in sugar beet leaves inoculated with Cercospora beticola (Bargabus et al. 2002). BTH treatment induced class III chitinases (PR-8 proteins) in cucumber inoculated with Colletotrichum orbiculare (Liu et al. 2008). Levels of PR-8 RNA were increased 10-fold in BTH-treated apple seedlings over levels in untreated seedlings (Maxon-Stein et al. 2002). PR-11 class of chitinase has been found to be rapidly induced in BTH-treated rice plants at 1 day after inoculation with the rice blast pathogen Magnaporthe oryzae (Ahn et al. 2005). Chitinases and glucanases show lytic activity against fungi and bacteria. BTH induced collapse of hyphae of the pathogen Venturia nashicola in pear leaves and the collapse of hyphae was accompanied by destruction of the fungal cell wall due to increased expression of the lytic enzymes (Jiang et al. 2008). β-1,3-glucanases and chitinases show high antifungal action synergistically (Mauch et al. 1988). BTH treatment generally induces both glucanase and chitinase activities and probably, induction of these groups of enzymes would have contributed for enhanced defense responses. Another PR protein commonly induced by BTH is PR-5 protein (Ramesh Sundar et al. 2001; Ziadi et al. 2001a; Suo and Leung 2002). PR-5 proteins show high antifungal activity (Woloshuk et al. 1991). They alter permeability of fungal membranes (Vigers et al. 1992). BTH treatment induces resistance in rose leaves against the black spot disease caused by Diplocarpon rosae. It was accompanied by the induction and accumulation of PR-5 protein, besides PR-1, PR-2, and PR-3 proteins (Suo and Leung 2002). Induction of PR-5 protein by BTH was observed in sugarcane plants (Ramesh Sundar et al. 2001). Ziadi et al. (2001a) reported that BTH treatment induced the accumulation of PR-5 protein in cauliflower seedlings inoculated with Peronospora parasitica. Class III peroxidases, which are induced during pathogenesis are considered as PR proteins belonging to PR-9 protein family (van Loon et al. 2006). BTH induced expression of peroxidases in various plants (Bargabus et al. 2002; Ramesh Sundar et al. 2001; Ajay and Baby 2010). PR-9 proteins contribute in making the plant cell wall harder for the pathogens to penetrate (Almagro et al. 2009). Induction of PR-10 proteins is a common phenomenon in BTH-treated plants (Ziadi et al. 2001b; Faize et al. 2004). BTH induced the accumulation of PR-10 protein in Japanese pear leaves (Faize et al. 2004). It strongly induced accumulation of PR-10 transcripts in apple leaves (Ziadi et al. 2001b). PR-10 protein shows ribonuclease activity (Vidhyasekaran 2007; Gómez-Gómez et al. 2011).

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3.2.9 Management of Fungal Diseases in Crop Plants by Triggering Immune Responses Using BTH BTH has been shown to control various fungal diseases in several crops by inducing defense genes. BTH induces systemic resistance and controls wheat powdery mildew caused by Blumeria graminis f. sp. tritici (Gorlach et al. 1996; Stadnik and Buchenauer 2000). It protects wheat systemically against powdery mildew infection by affecting multiple steps in the life cycle of the pathogen. The onset of resistance was accompanied by the induction of a number of wheat chemically induced (WCI) genes, including genes encoding lipoxygenase and a sulfur-rich protein (Gorlach et al. 1996). Inhibition of phenylalanine ammonia-lyase suppresses the resistance induced by acibenzolar-S-methyl in wheat, suggesting the role of phenylalanine ammonia-lyase in the induced resistance (Stadnik and Buchenauer 2000). Efficacy of BTH in control of powdery mildew of winter wheat plants has been demonstrated in large commercial fields in Poland (Glazek and Krzyzinska 1999). This treatment provided long-lasting protection for 7–8 weeks (Glazek and Krzyzinska 1999). BTH was effective in inducing resistance against barley powdery mildew pathogen Blumeria graminis (Faoro et al. 2008). BTH did not immediately induce ROS production, but conditioned the plants for a faster and stronger response upon infection with B. graminis (Faoro et al. 2008). This potentiated or “primed” response included a more intense HR-associated oxidative burst and more extensive formation of cell wall appositions coupled with greater accumulation of phenolic compounds at sites of attempted fungal penetration (Faoro et al. 2008). BTH controls powdery mildew (Golovinomyces cichoracearum) in lettuce (Matheron and Porchas 2003). BTH is effective in controlling rice blast caused by Magnaporthe oryzae (Ge et al. 2001). BTH induces resistance in cucumber against the anthracnose pathogen Colletotrichum lagenarium and the scab pathogen Cladosporium cucumerinum (Ishii et al. 1999). Resistance induced by BTH in cucumber against the scab pathogen C. cucumerinum was related to the rapid accumulation of chitinase (Narusaka et al. 1999). BTH induced resistance and reduced the number of lesions caused by Didymella bryoniae in cucumber cultivar SMR Wisconsin 58 (Da Rocha et al. 2001). However, it did not reduce the size of lesions. It suggests that BTH-induced resistance partially stopped the pathogen at penetration, but did not impede its spread. It caused stomata closing in the cultivar SMR Wisconsin 58 (Da Rocha et al. 2001). BTH protected beans against anthracnose (Colletotrichum lindemuthianum) when applied as seed and soil treatment (Bigirimana and Höfte 2002). Application of BTH induced resistance in sunflower against rust (Puccinia helianthi) infection (Prats et al. 2002). The reduced frequency of infection was due to a reduction in germination and appressorium formation of the rust pathogen. BTH treatment increased accumulation and excretion of coumarins and other phenolic compounds on the foliage. When the leaf exudates collected from BTH-treated plants were applied exogenously, germination and appressorium formation of urediospores were reduced (Prats et al. 2002). BTH controls damping-off (Rhizoctonia solani) of oilseed rape (Jensen et al. 1998).

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BTH applied as a soil drench (100 μg/ml) induced accumulation of PR proteins and phenolics and reduced the red rot lesion development in sugarcane caused by Colletotrichum falcatum (Ramesh Sundar et al. 2001). Canes from BTH-treated sugarcane fields were inoculated with the pathogen 30 days after treatment, and red rot lesion progression was assessed 10 days after inoculation. Lesion progression was confined to the inoculated internode and in the canes from untreated field it extended up to three internodes from the point of inoculation (Ramesh Sundar et al. 2001). BTH protects Japanese pear against rust (Gymnosporangium spp.) and scab (Venturia nashicola) (Ishii et al. 1999). BTH reduced the development of gray mold (Botrytis cinerea) of strawberry, when applied as 0.25 mg a. i. m l−1 (Terry and Joyce 2000). BTH effectively controlled papaya black spot caused by Asperisporium caricae (Oliveira and Nishijima 2014). It also induced systemic resistance against the pathogen and the level of protection was dose-dependent. Maximum level of protection against A. caricae was obtained with 25–100 μm BTH, with a time interval of 3 days between application of the activator and inoculation with the pathogen (Oliveira and Nishijima 2014). BTH treatment induced resistance in rose against Diplocarpon rosae, the black spot pathogen and it was accompanied by the induction and accumulation of various pathogenesis-related (PR) proteins such as PR-1, PR-2, PR-3, and PR-5 proteins (Suo and Leung 2002). BTH induced resistance against Alternaria macrospora leaf spot of cotton (Colson-Hanks and Deverall 2000). BTH reduced rhizoctonia leaf spot (Thanatephorus cucumeris) and frog eye leaf spot (Cercospora nicotianae) incidence in tobacco (Cole 1999). BTH-induced resistance of French bean to the rust fungus Uromyces appendiculatus involves an oxidative burst but no HR-related cell death (Iriti and Faoro 2003). BTH primes cowpea seedlings for rapid induction of resistance (Latunde-Dada and Lucas 2001). It induced systemic priming of PAL, chitinase activity, and phytoalexin accumulation in cowpea seedlings and enhanced resistance against the anthracnose pathogen Colletotrichum destructivum (Latunde-Dada and Lucas 2001). BTH significantly increased resistance against the rice blast pathogen Magnaporthe grisea, but was ineffective against the brown spot pathogen Cochliobolus miyabeanus in rice plants. Methyl jasmonate treatment was ineffective against both the pathogens. These results suggest that specific signaling pathway has to be activated to confer resistance against specific pathogen in a particular host (Ahn et al. 2005). BTH treatment significantly enhanced resistance against the fungal pathogen Leptosphaeria maculans in Brassica napus (Ahn et al. 2005). BTH induces resistance against the powdery mildew pathogen Sphaerotheca macularis in strawberry (Hukkanen et al. 2007). BTH treatment induced systemic acquired resistance in grapevine and reduced Botrytis cinerea infection in berries (Iriti et al. 2004).

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3.2.10 Management of Oomycete Diseases of Crop Plants by Triggering Plant Immune Responses Using BTH BTH has been shown to trigger defense responses against various oomycete pathogens. It protects sunflower plants against the downy mildew pathogen Plasmopara helianthi (Tosi and Zazzerini 2000). It controls tobacco blue mold caused by Peronospora tabacina (Johnson et al. 2004). It also controls downy mildew (Peronospora parasitica) of oilseed rape (Jensen et al. 1998). Downy mildew of maize (Peronospora sorghi) is effectively controlled by BTH (Morris et al. 1998). BTH effectively controlled the downy mildew disease caused by the oomycete pathogen Peronospora parasitica in cauliflower (Ziadi et al. 2008). Time of application of BTH has been reported to be important in inducing resistance against the oomycete pathogen. BTH has to be applied much before challenge inoculation with the pathogen. The infection by the downy mildew pathogen P. parasitica was very much reduced when the cauliflower plants were inoculated with the pathogen 2 days after BTH treatment (Ziadi et al. 2008). The combination of BTH applications with the standard fungicide program was more efficacious than either fungicides or BTH alone in reducing the number of blue mold lesions caused by Peronospora tabacina in tobacco (LaMondia 2008). BTH controls the downy mildew disease caused by the oomycete pathogen Peronospora belbahrii in basil (Ocimum basilicum) (Mersha et al. 2013). The area under the disease progress curve (AUDPC) of disease severity was significantly reduced compared to the non-treated control when BTH was sprayed or drenched at rates of 25–400 mg/l (Mersha et al. 2013). BTH induced resistance against Phytophthora palmivora in papaya (Zhu et al. 2003). It effectively controls P. palmivora in papaya by intervening in pathogenesis of the oomycete (Qiu et al. 2004). BTH effectively controlled Phytophthora blight caused by Phytophthora capsici in squash (Cucurbita pepo). BTH applied as a soil drench at 30 mg l−1 provided the greatest protection with no symptoms developed on treated squash plants (Zhang et al. 2011).

3.2.11 Management of Bacterial Diseases in Crop Plants by Triggering Plant Immune Responses Using BTH BTH has been shown to trigger immune responses against bacterial pathogens and it effectively controls several bacterial diseases in various crop plants. BTH treatment significantly enhanced resistance against the bacterial pathogen Pseudomonas syringae pv. maculicola in Brassica napus (Potlakayala et al. 2007). BTH treatment induced resistance to the tomato bacterial leaf spot pathogen Xanthomonas vesicatoria (Cavalcanti et al. 2006). It also controlled bacterial canker caused by Clavibacter michiganensis subsp. michiganensis in tomato (Baysal et al. 2003; Soylu et al. 2003). BTH treatment induces resistance against the bacterial pathogen Pseudomonas syringae pv. tomato in Arabidopsis (Lawton et al. 1996). BTH treatment

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induced resistance to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae in rice (Babu et al. 2003a, b). About 50% reduction in the bacterial blight disease intensity was observed in rice plants treated with BTH at 100 μg a.i./ml (Babu et al. 2003a). Under field conditions, BTH reduced severity of Xanthomonas leaf blight of onion caused by Xanthomonas axonopodis pv. allii (Lang et al. 2007). BTH induces resistance against the fire blight pathogen Erwinia amylovora on apple (Baysal and Zeller 2004). BTH induces resistance against pepper bacterial spot disease caused by Xanthomonas campestris pv. vesicatoria (Buonaurio et al. 2002). BTH treatment completely prevented occurrence of typical symptoms of the bacterial spot caused by X. campestris pv. vesicatoria. However, necrotic spots typical of a hypersensitive response (HR) were observed on plants treated with BTH. Application of bacteriophages in combination with BTH suppressed a visible HR and provided excellent disease control (Obradovic et al. 2005). The results suggest that integrated use of BTH and bacteriophages may be an effective strategy against the bacterial spot of tomato. BTH was highly effective in controlling pepper bacterial spot caused by Xanthomonas campestris pv. vesicatoria when it was applied as a mixture of BTH and copper hydroxide (2.5 + 40 g h l−1 active ingredient) (Buonaurio et al. 2002). BTH effectively reduced bacterial speck (Pseudomonas syringae pv. tomato) incidence in greenhouse-grown tomatoes (Herman et al. 2008). When BTH was sprayed on tomato leaves, it induced resistance against the bacterial leaf spot pathogen Xanthomonas vesicatoria in tomato (Cavalcanti et al. 2006, 2007). BTH effectively controls tobacco wild-fire disease caused by Pseudomonas syringae pv. tabaci (Cole 1999). BTH induced resistance against bacterial head rot disease of broccoli caused by Pseudomonas marginalis and Pseudomonas fluorescens (Pajot and Silué 2005). BTH treatment reduced the fire blight (Erwinia amylovora) disease severity in apple trees (Brisset et al. 2000; Maxson and Jones 2002). Seedling treatment of tomato plants with BTH significantly reduced disease severity of bacterial wilt caused by Ralstonia solanacearum (56% disease reduction). Application of BTH increased seedlings biomass relative to infected control by 64.3% (Abo-Elyousr et al. 2012). BTH was effective in controlling bacterial wilt (R. solanacearum) of tomato only under low disease pressure. It was not effective under high inoculum potential (Hacisalihoglu et al. 2006). BTH induces resistance against Pseudomonas syringae pv. lachrymans in cucumber (Ku´zniak et al. 2014).

3.2.12 Management of Virus Diseases in Crop Plants by Triggering Plant Immune Responses Using BTH BTH is useful in controlling virus diseases which are difficult to be controlled by traditional chemical methods. BTH has been shown to be effective in controlling various virus diseases. BTH effectively controlled TSWV infection in flue-cured tobacco plants (Mandal et al. 2008). The efficacy of BTH varied depending on the

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dosage of BTH applied. As the dosage of BTH increased from 0.25 to 4 g a.i./7000 plants, incidence of plants showing local and systemic infection and the relative levels of TSWV in the treated plants decreased. At 4 g of BTH, the highest level of disease resistance was observed compared with other lower dosage. But at this dose plants showed the highest level of phytotoxic symptoms on the treated leaves and overall stunting of plants. It has been shown that the concentration of BTH should be 2 g a.i./7000 plants to obtain significant disease control with less phytotoxicity symptoms. It has also been shown that tobacco seedlings should be treated with BTH prior to their transplant in the field since little benefit was seen treating older plants (Mandal et al. 2008). BTH induces systemic resistance against TSWV in tobacco. Activation of resistance was observed within 2 days after treatment with BTH and a high level of resistance was observed at 5 days onward after treatment with BTH (Mandal et al. 2008). BTH treatment reduced virus replication and movement (Mandal et al. 2008). Several field trials were conducted to assess the efficacy of BTH in the control of TSWV in tobacco in Georgia, USA. BTH significantly reduced TSWV incidence in all locations (Csinos et al. 2001). Preplant application of BTH and imidacloprid resulted in smaller areas under disease progress curve (AUDPC), and higher yields compared with the nontreated controls in all the field trials conducted for four years in USA (Nischwitz et al. 2008). Efficacy of BTH in controlling TSWV incidence in flue-cured tobacco has been demonstrated in several other field trials (Pappu et al. 2000; McPherson et al. 2005). Foliar application of BTH reduced the incidence of TSWV in tomato in two field trials conducted in North Florida, USA during the years 2000 and 2002 when natural infection pressure was high. BTH treatment reduced the primary spread of the disease in tomato. It reduced the incidence of TSWV by 28% in both the field trials (Momol et al. 2004). BTH treatment was very effective in controlling TMV infection in tobacco. BTH induced systemic acquired resistance against TMV in tobacco (Parkunan et al. 2013). BTH-treated tobacco plants did not show any mosaic disease symptoms (Friedrich et al. 1996). Viral RNA accumulation in BTH-treated plants was reduced by 95%, when compared to the untreated plants. In all treated plants, there was no sign of lesions associated with TMV infection (Friedrich et al. 1996). There was about 60% reduction in TMV incidence in tobacco in the different field trials (Oostendorp et al. 2001). However, the time of application determined the efficacy of BTH in controlling TMV infection in tobacco. Inoculation of tobacco plants with the mixtures of BTH and the virus did not show any inhibition of the number and size of the local lesions. The protective effect increased day by day and 6–7 days after BTH treatment the production of local lesions was inhibited almost completely (Pospieszny and Folkman 2000). BTH treatment has been found to be effective in inducing resistance against Potato virus X (PVX) and Potato virus Y (PVY) in potato crops (Burketová et al. 2000). The efficacy of BTH in management of PVY, Cucumber mosaic virus (CMV) and TSWV viruses in tomato crops has been reported in the field trial conducted in Italy (Fanigliulo et al. 2009). BTH treatment induced resistance also against PVY in tobacco crops (Oostendorp et al. 2001).

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Rhizomania of sugarbeet is an economically important disease caused by Beet necrotic yellow vein virus (BNYVV). The name rhizomania means ‘root madness’ or crazy root and refers to the extensive proliferation of lateral roots (Hill and Torrance 1989). The virus is transmitted by the soilborne plBTHodiophorid Polymyxa beta, which survives in infested soil for many years in the form of thick-walled fungal resting structures called cytosori (Wisler et al. 1999; Burketová et al. 2003). Rhizomania is widely prevalent in California and in other beet-growing states in USA and in England (Hill and Torrance 1989; Wisler et al. 1994, 1999). Chemical control of the virus transmitted by a soil-borne vector is almost impossible (Wisler et al. 1999). BTH, which triggers immune responses through action of ROS-SA signaling system, has been shown to have potential to manage rhizomania disease (Burketová et al. 2003). BTH applied as a seed treatment at 0.5 a.i./kg seed reduced BNYVV titer compared to an untreated control in a BNYVV-tolerant sugarbeet cultivar, but not in a susceptible cultivar (Mouhanna and Schlösser 1998). Irish yellow spot virus (IYSV) is a threatening disease in onion worldwide (Gent et al. 2004a, b, 2006). BTH appears to have potential for management of this virus disease in onion. The potential value of BTH for control of IYSV in onion crop was demonstrated by Gent et al. (2004b) in the field trial conducted in Colorado (USA), in which a 34% reduction in incidence of plants with symptoms of iris yellow spot was observed, compared with untreated controls, following four applications of BTH. There was also a corresponding increase in jumbo grade bulbs in the BTH-treated plots (Gent et al. 2004b). BTH has been registered for use in onions to manage IYSV in USA (Lang et al. 2007). BTH was able to induce resistance against Alfalfa mosaic virus (AlMV) in bean plants (Pospieszny and Folkman 2000). Bean and tomato plants pretreated with BTH were effectively protected against systemic infection by Tomato black ring virus (TBRV) (Pospieszny and Folkman 2000). BTH treatment induced resistance against Mungbean yellow mosaic virus (MYMV) in blackgram (Vigna mungo) and increased the crop yield compared with untreated plants under field conditions (Venkatesan et al. 2010). BTH induces systemic resistance in tomato to Cucumber mosaic virus (Anfoka 2000). Collectively these studies suggest that BTH may be a potential tool for management of virus diseases in crop plants, for which no reliable chemical control is available.

3.2.13 Management of Phytoplasma Diseases of Crop Plants by Triggering Plant Immune Responses Using BTH Phytoplasmas are cell-wall-less bacteria belonging to the class Mollicutes. They are phloem-limited pathogens that cause different symptoms such as yellowing, stunting, proliferation, phyllody, virescence, and general decline (D’Amelio et al. 2010). They are transmitted from plant to plant mostly by leafhoppers. The phytoplasmas are obligate parasites of plants and insect vectors (Bressan and Purcell 2005). The phytoplasmas reproduce within tissues of their insect vectors and are transferred

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in the salivary secretions to new host plants during feeding (Olivieri et al. 2009). Because of their cryptic nature, phytoplasmas are difficult to manage. BTH has been shown to be a powerful weapon to control phytoplasma diseases. BTH application delayed symptom development and reduced the symptoms severity of yellows, the phytoplasma disease in chrysanthemum. It reduced the multiplication of ‘Candidatus Phytoplasma asteris’ (CYP), the causal agent of chrysanthemum yellows (D’Amelio et al. 2010). The disease severity was significantly lower for the first two weeks post-inoculation of the pathogen in BTH-treated plants compared with the control ones. BTH application was ineffective in reducing CYP transmission efficiency of the leafhopper vector Macrosteles quadripunctulatus. The survival of the vector was unaffected by feeding on BTH-treated plants. However, BTH treatment reduced multiplication of the phytoplasma in the host plant. The results suggest that BTH may reduce multiplication of the phytoplasma by inducing host defense responses against the phytoplasma, and not by interfering with the transmission efficiency of the vector (D’Amelio et al. 2010). In contrast, Bressan and Purcell (2005) reported a significant effect of BTH in reducing X-disease phytoplasma transmission efficiency of the leafhopper vector Colladonus montanus. Induction of resistance against various insects by BTH has been reported (Inbar et al. 1998; Nombela et al. 2005). Bois noir is the common phytoplasma disease of grapevine. This is caused by a Candidatus Phytoplasma solani and transmitted by the vector Hyalesthes obsoletus. The disease is widespread in the viticultural areas in Italy (Romanazzi et al. 2009). No effective control measure against the phytoplasma disease is known. The plant defense inducer BTH applied as foliar spray at weekly intervals significantly controlled the phytoplasma infection and the diseased plants showed increased recovery due to BTH treatment (Romanazzi et al. 2009, 2013). These studies have indicated the potential of BTH to manage phytoplasma diseases.

3.2.14 Management of Parasitic Plants by Manipulation of ROS Signaling System Using BTH The root parasitic plants Orobanche species threaten agricultural production in many parts of the world. At present, no commercially available chemical herbicide, which can combat the parasitic plant with sufficient margin of selectivity and efficiency, is available (Sauerborn et al. 2002). BTH, which triggers ROS production, induces defense genes and resistance to Orobanche cumana (Sauerborn et al. 2002). Sunflower seeds were treated with different concentrations of BTH. The number of successful attachments of O. cumana to sunflower roots decreased upon BTH seed soaking (Fig. 3.8; Sauerborn et al. 2002). BTH induced resistance against O. cumana and restricted the broomrape attachment to the host root and retarded tubercle formation and development (Buschmann et al. 2005). BTH treatment induced an oxidative burst before an attack by O. cumana. An accumulation of H2 O2 has been reported in BTH-treated healthy sunflower roots (Sauerborn et al. 2002). BTH treatment also

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35 30 25

Number of 20 Orobanche cumana 15 shoots/pot 10 5 0 Control

BTH treatment

Fig. 3.8 Efficacy of BTH treatment in controlling Orobanche cumana infection in sunflower (Adapted from Sauerborn et al. 2002)

induced the phytoalexin scopoletin and salicylic acid-inducible chitinase (class III chitinase) in sunflower roots (Sauerborn et al. 2002). The phytoalexin has been suggested to be involved in conferring resistance to the root parasite (Wegmann et al. 1991) and the chitinase is considered as a marker for SAR (Systemic Acquired Resistance) in plants (Sauerborn et al. 2002). These results suggest that BTH can be exploited to manipulate ROS signaling system to intervene in infection by parasitic plants. BTH induced resistance in oilseed rape (Brassica napus) against the parasitic higher plant broomrape (Orobanche ramosa). BTH was applied as foliar sprays or soil drenches at 0.05 g a.i. l−1 at bi-weekly intervals. Both foliar and soil applications of BTH reduced broomrape attachment by 70% and prevented the loss of crop biomass (Véronési et al. 2008). BTH treatment decreased branched broomrape (O. ramosa) infection even up to 80% in hemp and tobacco (Gonsior et al. 2004). Foliar application of 0.6–1.0 mM BTH reduced broomrape infection in faba bean by limiting the success in attachment and retarding the development of established tubercles (Pérez-deLuque et al. 2010). BTH induced resistance against Orobanche minor in red clover (Trifolium pretense). Roots of red clover grown in plastic chambers were applied with BTH and then inoculated with O. minor seeds. Attachments of the parasite were observed after 5 weeks. BTH significantly reduced the number of established parasites by more than 75% (Fig. 3.9; Kusumoto et al. 2007). The concentrations of BTH, which are highly effective in controlling disease, generally exhibit phytotoxicity. BTH at high concentrations may be highly effective in completely controlling Orobanche spp. However, the most effective dose of BTH may be phytotoxic to plants. BTH applied in concentration of 10 mg/pot applied as soil drench three times in interval of 14 days, resulted in a complete inhibition of O. cumana infection in sunflower roots. However, at 10 mg/pot treatment, the weight

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Number of 100 Orobanche minor seedlings 80 establishing parasitism 60 40 20 0 Control

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Fig. 3.9 Efficacy of BTH in management of Orobanche minor infection in red clover (Adapted from Kusumoto et al. 2007)

and size of the sunflower heads were diminished by about 70% in contrast to nonparasitized and untreated control. When BTH was applied at low concentration of 5 mg/pot, it reduced O. cumana development in the host sunflower by about 87% and at this low concentration no phytotoxicity symptoms were observed on sunflower (Fan et al. 2003). The results suggest that BTH is able to decrease infection with O. cumana when given as soil drench and when applied in low concentrations the compound reduces the root parasitic plant infection without reducing production potential of the crop. BTH, applied three times as soil drench at 14 days interval commencing 14 days after host sunflower plant emergence, effectively controlled the broomrape infestation in sunflower. However, this treatment reduced biomass of sunflower plants (Buschmann et al. 2005). In order to reduce the negative effects of BTH on sunflower biomass and to increase the efficacy of O. cumana control, the application times were varied. When BTH was applied only two times, by delaying the first application to 28 days after host emergence, there was no adverse effect on sunflower biomass production and also on the broomrape control (Buschmann et al. 2005). Alternatively, when BTH was applied as foliar spray, it effectively controlled the broomrape infection in sunflower without any phytotoxic effects on the host plant (Buschmann et al. 2005). These results suggest that the phytotoxicity induced by BTH can be managed by selecting suitable application technologies.

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3.3 Manipulation of ROS and Redox Signaling Systems Using Riboflavin to Promote Plant Immunity Potential for Crop Disease Management Riboflavin (vitamin B2 ) is a water-soluble vitamin and is an antioxidant (Dong and Beer 2000; Taheri and Höfte 2006). It is involved in antioxidation and peroxidation and both processes affect the production of ROS. Riboflavin treatment induced ROS signaling system and specifically H2 O2 production in rice after challenge inoculation with the rice sheath blight pathogen Rhizoctonia solani (Taheri and Höfte 2006). Riboflavin induced systemic resistance against both the rice sheath blight pathogen R. solani and the aggregate sheath spot pathogen R. oryzae-sativa (Taheri and Höfte 2006, 2007a, b). Exogenous application of riboflavin (added to soil at 40 mg/kg) induced resistance against the blast pathogen Magnaporthe oryzae in rice plants. When riboflavin was added to spores of the pathogen, it showed toxicity towards the spores. Antioxidant reagents such as superoxide dismutase, catalase, and scavengers of hydroxyl radical protected the spores from intoxication. The results suggest that riboflavin induces resistance against the pathogens by producing ROS (Aver’yanov et al. 2000). The induced ROS signaling system activated cationic peroxidase and formation of lignin in rice (Taheri and Höfte 2006). Riboflavin induced resistance against Fusarium wilt (Fusarium oxysporum f. sp. ciceri) and charcoal rot (Macrophomina phaseolina) of chickpea. It did not enhance level of SA levels, but induced activities of peroxidase and phenylalanine ammonia-lyase, and accumulation of phenolics, and PR proteins (Saikia et al. 2006). Seed-soak treatment with riboflavin at 20 mM enhanced seed germination and seedling vigor and induced downy mildew (Sclerospora graminicola) disease resistance in pearl millet (Pushpalatha et al. 2007). The induced resistance persisted throughout the crop growth period. The vitamin treatment had a growth promotional effect and it increased the crop yield (Pushpalatha et al. 2007). Foliar application of riboflavin induces resistance against several diseases of tobacco and Arabidopsis (Dong and Beer 2000). The protein kinase inhibitor and mutation in the NPR1 gene impaired responsiveness to riboflavin. Riboflavin induced resistance and defense gene expression in transgenic tobacco and Arabidopsis plants expressing the bacterial NahG gene, which fail to accumulate SA. In contrast, riboflavin failed to induce resistance in plants treated with protein kinase inhibitor K257a. It also did not induce disease resistance in NPR1 mutant plants (Dong and Beer 2000). These results suggest that riboflavin-induced resistance depends on protein kinase activity and function of the regulatory gene NPR1. In contrast, this pathway appears to function independent of SA signaling system (Dong and Beer 2000). Mixture of riboflavin (26.6 μM) and methionine (1 mM) was found to be highly effective in controlling flyspeck (Schizothyrium pomi) and sooty blotch (a disease complex induced by at least three fungi: Peltaster fructicola, Leptodontium elatius and Geastrumia polystigmatis) diseases in apple (Andrews et al. 2001). Riboflavin was found to induce systemic resistance against Tobacco mosaic virus in tobacco

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(Fig. 3.10; Dong and Beer 2000). It also induced systemic resistance against the fungal pathogen Alternaria alternata in tobacco (Dong and Beer 2000). It also induced systemic resistance against the oomycete (Hyaloperonospora parasitica) and bacterial (Pseudomonas syringae pv. tomato) pathogens in Arabidopsis thaliana (Dong and Beer 2000). It induced resistance against the rice blast pathogen Magnaporthe oryzae and effectively controlled the blast disease (Aver’yanov et al. 2000). Riboflavin enhanced resistance in Arabidopsis and tobacco by 40–70%. Riboflavininduced resistance is persistent and continues to be effective against Alternaria alternata in tobacco for 40 days. Riboflavin-induced resistance is nonspecific and provides protection against wide range of pathogens (Dong and Beer 2000). Unlike SA and INA which are phytotoxic at the concentration needed to induce resistance, riboflavin is not phytotoxic at concentrations much higher than that needed for resistance induction (Dong and Beer 2000; Saikia et al. 2006). These results reveal that riboflavin is a safe tool to manage crop diseases. Riboflavin was not able to enhance defense responses. However, when riboflavin pretreated plants were challenge inoculated with pathogens, accumulation of defenserelated compounds was observed (Saikia et al. 2006; Taheri and Höfte 2006). Riboflavin does not cause either macroscopic or microscopic cell death in plants at concentrations that effectively induce resistance. Thus, it appears that it activates resistance mechanisms in a HR-independent manner (Dong and Beer 2000; Saikia et al. 2006). Riboflavin induces disease resistance in the absence of hypersensitive cell death in plants (Zhang et al. 2009). It induces priming of defense responses. Riboflavin treatment alone did not induce disease resistance response in Arabidopsis. Similarly 200 180 160 140 120

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100

Upper leaves

80 60 40 20 0

Water

Riboflavin

Water or riboflavin was sprayed on lower leaves (treated) of plants. Seven days later the upper two leaves were inoculated with Tobacco mosaic virus

Fig. 3.10 Efficacy of riboflavin to induce systemic resistance against Tobacco mosaic virus (Aadapted from Dong and Beer 2000)

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inoculation with virulent bacterial pathogen alone could not induce disease resistance response. However, both riboflavin treatment and challenge inoculation with the pathogen triggered defense response (Zhang et al. 2009). Riboflavin-mediated induced disease resistance was associated with H2 O2 burst. The priming process needed NPR1 and maintenance of H2 O2 burst but was independent of SA, JA, ET, and ABA, the well-known pathways of hormone signal transduction (Zhang et al. 2009).

3.4 Molecular Manipulation of ROS-Mediated Redox Signaling System Using Menadione Sodium Bisulphite for Crop Disease Management Menadione sodium sulphite (MSB) is a water-soluble addition compound of vitamin K3 . It induces resistance against the banana wilt pathogen Fusarium oxysporum f. sp. cubense (Borges-Pérez and Fernandez-Falcon 1996). MSB induced systemic resistance against A-type Leptosphaeria maculans, the fungal pathogen causing phoma stem canker in oilseed rape (Brassica napus) (Fig. 3.11; Borges et al. 2003). There was no visible evidence of a HR on MSB-pretreated plants inoculated with L. maculans. MSB pretreatment had no direct effect on PR-1 expression in oilseed rape. The treatment significantly enhanced ascorbate peroxidase gene (APX) expression in the pathogen-inoculated plants. MSB induces resistance in oilseed rape plants independent of PR-1, a marker gene for SA signaling system, in a way that may involve enhanced production of ROS. Menadione, a redox-active compound, is a ROS generator, readily undergoing cell-mediated one-electron reduction, producing superoxide radicals (O2 − ) and H2 O2 (Hassan and Fridovich 1979). MSB, a derivative 4.5 4 3.5 3

Average number of lesions

2.5 2 1.5 1 0.5 0 Water

MSB

Fig. 3.11 Efficacy of menadione sodium sulphite (MSB) in inducing resistance against Leptosphaeria maculans in oilseed rape plants. (Adapted from Borges et al. 2003)

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of menadione, could be a similarly effective ROS generator and therefore exert an oxidative stress (Borges et al. 2003). MSB treatment induces systemic resistance by activating redox signaling systems, without inducing necrotic HR lesions. Therefore, the induced resistance by MSB may not affect the yield potential of the plants. MSB was nonphytotoxic both on oilseed rape plants treated with a 200 μM concentration and on banana plants treated with 1300 ppm, 21 times more concentrated spray than that used on oilseed rape (Borges et al. 2003). These studies suggest that MSB is a potential tool to manage crop diseases.

3.5 Management of Crop Diseases Using Thiamine Through Manipulation of ROS Signaling System Vitamin B1 (thiamine) treatment (10 mM) induced systemic acquired resistance in susceptible plants through priming (Ahn et al. 2007). Thiamine did not induce cellular and molecular defense responses in Arabidopsis; however, subsequent challenge inoculation with the bacterial pathogen Pseudomonas syringae pv. tomato triggered transcription of various defense genes. Vitamin B1 treatment and subsequent pathogen invasion induced ROS accumulation. Removal of H2 O2 by catalase almost completely nullified cellular and molecular defense responses including expression of the PR protein gene PR1 and phenylalanine ammonia-lyase encoding gene PAL1 and callose accumulation (Ahn et al. 2007). Catalase also nullified the vitamin B1induced resistance against the bacterial pathogen (Fig. 3.12; Ahn et al. 2007). These results suggest that vitamin B1 is a potential tool to manage pathogens through its action on ROS signaling system. Thiamine has been shown to induce resistance against the downy mildew pathogen Plasmopara viticola in grapevine (Boubakri et al. 2012). 9 8 7 6

Bacterial growth (Log CFU/g)

5 4 3 2 1 0 Control

Thiamine

Thiamine+catalase

Fig. 3.12 Effect of catalase on bacterial growth in Arabidopsis treated with thiamine and challenged with Pseudomonas syringae pv. tomato (Adapted from Ahn et al. 2007)

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3.6 Manipulation of ROS and Redox Signaling Systems Using Herbicides to Activate Plant Immune Signaling System for Crop Disease Management 3.6.1 Management of Crop Diseases Using Lactofen Through Singlet Oxygen-Mediated ROS Signaling System Some herbicides have been shown to act as plant innate immunity system activators. Lactofen is member of the diphenylether class of herbicides. It targets protoporphyrinogen oxidase, which in turn causes singlet oxygen generation (Graham 2005). Singlet oxygen is involved in triggering ROS-mediated signaling system. Lactofen induces programmed cell death in soybean and phenolics accumulation accompanies cell death. Expression of several defense-related genes including chalcone synthase, chalcone reductase and isoflavan synthase genes is enhanced due to lactofen treatment. Lactofen triggers massive isoflavone accumulations and activates biosynthesis of the phytoalexins glyceollins. It also triggers expression of PR-1a, PR-5 and PR-10 genes in soybean (Graham 2005). Application of lactofen to soybean reduces the severity of Sclerotinia white mold damage in the field (Dann et al. 1999). The soybean isoflavonoid phytoalexin glyceollin accumulates in lactofen-treated leaves (Nelson et al. 2002). Lactofen induced massive accumulation of several isoflavones, including daidzein and genistein (Graham and Graham 1999). Lactofen predominantly induces the accumulation of free isoflavone aglycones rather than their conjugates (Landini et al. 2002). Cobra 2 EC is a lactofen and it induces resistance against pathogens. It is a strong inducer of soybean isoflavones and elicits the phytoalexin glyceollin accumulation in soybean leaves (Bean and Graham 2001). Cobra 2 EC plus adjuvant applications provided significant control of Sclerotinia sclerotiorum and Phytophthora sojae in various field trials (Bean and Graham 2001).

3.6.2 Management of Crop Diseases Using Trifluralin Through Manipulation of ROS-Mediated Redox Signaling System Trifluralin is a dinitroaniline herbicide. Low concentrations of trifluralin induce disease resistance against several pathogens. Trifluralin induces resistance against the wilt pathogen Fusarium oxysporum f. sp. melonis in melon. It has been suggested that ethylene signaling system may be involved in inducing resistance. Redox signaling system may also be involved and trifluralin induces higher accumulation of glutathione (Cohen et al. 1986). Higher glutathione levels following trifluralin treatment have been suggested to confer protection against Fusarium oxysporum f. sp. melonis in melon plants (Bolter et al. 1993). Trifluralin treatment induced enhanced

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expression of several defence-related genes in melon and induced resistance to Fusarium wilt caused by Fusarium oxysporum f. sp. melonis (Lotan-Pompan et al. 2007). Trifluralin treatment induced resistance to the wilt pathogen Fusarium oxysporum f. sp. lycopersici in tomato seedlings (Grinstein et al. 1984).

3.6.3 Management of Crop Diseases Using Glufosinate Ammonium Through Manipulation of ROS-Signaling System Glufosinate ammonium is a nonselective herbicide and it kills various kinds of plants including crop plants (Ahn 2008). The bar gene, which codes for the enzyme phosphinothricin acetyl transferase, is one of the most prevalent selectable markers of genetically engineered crops and confers tolerance against glufosinate ammonium. Hence, the herbicide can be used for management of several weeds in the field where transgenic crop plants are grown. The herbicide, besides controlling weeds induces resistance against various pathogens. Glufosinate ammonium treatment onto transgenic rice expressing bar gene showed resistance against rice blast (Magnaporthe oryzae) and rice sheath blight (Rhizoctonia solani) (Uchimiya et al. 1993; Tada et al. 1996). It also induced resistance against brown patch (Rhizoctonia solani) and dollar spot (Sclerotinia homoeocarpa), in bar-transgenic bentgrass (Higgins et al. 2003). Glufosinate ammonium induced high accumulation of H2 O2 in bar-transgenic rice plants. In transgenic control rice plants inoculated with M. oryzae, hydrogen peroxide did not accumulate at the infection site 24 h post inoculation (hpi) and began to be observed at 72 hpi. In transgenic rice, glufosinate ammonium induced hydrogen peroxide within 24 posttreatment. In the transgenic rice pretreated with glufosinate ammonium, most cells exhibited hydrogen peroxide accumulation and M. oryzae infection did not affect this cellular response (Ahn 2008). It induced SAand NPR1-dependent signaling systems and triggered the expression of transcription of various PR genes. The PR-1 transcription process induced by glufosinate ammonium was dependent on SA signaling system and independent of JA and ethylene signaling systems (Ahn 2008). Glufosinate ammonium induced resistance against the blast pathogen Magnaporthe grisea (= Magnaporthe oryzae) in transgenic rice, probably by activating ROS-dependent SA signaling system (Ahn 2008). Glufosinate ammonium treatment induced transcriptions of PR1, PBZ1, and POX22.3 genes in transgenic rice (Ahn 2008).

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3.7 Management of Crop Diseases Using Giant Knotweed Extract Through Activation of ROS Signaling System An ethanolic extract of the giant knotweed, Reynoutria sachalinensis, has been shown to act as plant innate immunity system activator. It was formulated as a commercial product and released as a wettable powder by the Gmgh Company, Munster, Germany in early 1990 s. It was registered under the trade name Milsana® . An aqueous formulation of concentrated extracts (Milsana flussig) has been found useful in controlling diseases (Daayf et al. 1995). Aqueous formulations were also developed and marketed by KHH BioSci., Inc., and Biofa AG companies (Wurms et al. 1999; Randoux et al. 2006). Milsana was developed as suspension concentrate and renamed as Regalia™ and marketed by Marrone Organics, U.S.A. Two liquid formulations of R. sachalinensis extract (Milsana® VP1999 and VP2000) have also been developed (Petsikos-Panayotarou et al. 2002). Besides Milsana, a water-soluble extract of R. sachalinensis has been shown to be effective against wheat powdery mildew caused by Blumeria graminis f. sp. tritici (V˘echet et al. 2005). Milsana treatment activates reactive oxygen species (ROS)-mediated signaling system. It enhanced the accumulation of H2 O2 at the penetration site by Blumeria graminis f. sp. tritici in wheat leaves (Randoux et al. 2006). Milsana triggers increases in the activities of peroxidases and β-1,3-glucanases in cucumber leaves. It also induces accumulation of phenolics (Daayf et al. 1995, 1997). Extracts from R. sachalinensis treatment induced the first enzyme of phenylpropanoid pathway, phenylalanine ammonia lyase (PAL) and optimal PAL activity was reached 25 h post-elicitation in cucumber leaves elicited with the plant extract (Schneider and Ullrich 1994). Collectively, these results suggest that Milsana elicits the flavonoid metabolism and induces accumulation of the defense-related flavonoid compounds, triggering resistance against the powdery mildew pathogen in cucumber. The pathogen itself can induce the defense responses; however, the plant extract primes the plants to enhance the activities of defense-related enzymes to a higher level in pathogen-inoculated tissues. The ultrastructural studies on the interaction between cucumber and powdery mildew pathogen revealed that the fungal haustoria and mycelia had collapsed after Milsana treatment, probably due to defense-related accumulation of an electrondense material around the infectious structure (Wurms et al. 1999). Milsana treatment induced accumulation of phenolic compounds in cucumber cultivars infected with the powdery mildew fungus (Daayf et al. 2000). Extracts from R. sachalinensis treatment induced the first enzyme of phenylpropanoid pathway, phenylalanine ammonia lyase (PAL) and optimal PAL activity was reached 25 h post-elicitation in cucumber leaves elicited with the plant extract (Schneider and Ullrich 1994). Milsana treatment induced flavonoid compounds (phytoalexins) in larger quantities than in water-treated control cucumber plants inoculated with the powdery mildew pathogen (Fofana et al. 2002). Milsana-induced flavonoid accumulation in cucumber was associated with an increased transcript accumulation of two flavonoid biosynthetic genes, chalcone synthase (CHS) and chalcone isomerase

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(CHI) and increased activities of these enzymes (Fofana et al. 2002). Milsana treatment enhanced the mRNA accumulation and the enzyme activity of both CHS and CHI in a coordinated manner (Fofana et al. 2002). Milsana is generally effective in controlling powdery mildew diseases in crop plants. It effectively controls powdery mildew diseases in wheat, cucumber, tomato, rose and begonia (Daayf et al. 1995, 1997; Pasini et al. 1996; KonstantinidouDoltsinis and Schmidtt 1998; Isebaert et al. 2002; V˘echet et al. 2005; KonstantinidouDoltsinis et al. 2006; Randoux et al. 2006). Milsana treatment effectively controlled powdery mildew (Sphaerotheca fuliginea) disease incidence in cucumber. However, Milsana induced only localized resistance, unlike another plant immunity activator Acibenzolar-S-methyl which induced both localized and systemic resistance in cucumber (Wurms et al. 1999). Milsana treatment on cucumber led to a 90% efficiency that was comparable to the efficiency of classical fungicide treatments in controlling powdery mildew (Konstantinidou-Doltsinis and Schmidtt 1998). It reduced powdery mildew severity even in highly susceptible cucumber cultivars (Petsikos-Panayotarou et al. 2002). Milsana flussig applied weekly at a concentration of 2% provided control of powdery mildew (S. fuliginea) on long English cucumber that was as effective as the standard fungicide benomyl (Daayf et al. 1995). Powdery mildew developed rapidly and affected 100% of the leaf area within 8 weeks on control plants. Both Milsana and the standard fungicide benomyl kept severity at less than 20% after transplanting. Subsequently, the efficacy of benomyl appeared to break down. This resulted in rapid development of disease severity that reached 100% after 8 weeks. In contrast, disease severity in Milsana-treated plants was only 50% at the end of the experiment in spite of high inoculum level (Daayf et al. 1995). Milsana treatment did not show any phytotoxic symptoms (Daayf et al. 1995). Milsana treatment induced resistance against the powdery mildew pathogen Blumeria graminis f. sp. tritici in wheat (V˘echet et al. 2005; Randoux et al. 2006). Milsana VP1999 and 2000 reduced powdery mildew incidence in tomato by about 50% and its efficacy was comparable to the standard fungicide, wettable sulfur (Konstantinidou-Doltsinis et al. 2006). R. sachalinensis leaf extract induced resistance against powdery mildew in wheat. The induced resistance in wheat was longlasting and the plant extract halted mildew disease progress at least up to 27 days after application (V˘echet et al. 2009).

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3.8 Manipulation of ROS Signaling System Using β-Aminobutyric Acid for Crop Disease Management 3.8.1 BABA Triggers ROS Production and Activates Plant Immune Responses The nonprotein amino acid β-aminobutyric acid (BABA) has been shown to induce resistance against several fungal (Olivieri et al. 2009; Barilli et al. 2010, 2015: Zhang et al. 2011), oomycete (Cohen et al. 1999; Reuveni et al. 2001; Silue et al. 2002; Pajot and Silu˙e 2005; Altamiranda et al. 2008; Nandeeshkumar et al. 2009; Olivieri et al. 2009; Cohen et al. 2010, 2011; Dubreuil-Maurizi et al. 2010; Liljeroth et al. 2010; Bengtsson et al. 2014a) and bacterial (Baysal et al. 2006; Hassan and Buchenauer 2007; Kamble and Bhargava 2007; Marcucci et al. 2010) pathogens in various crop plants. BABA has been shown to induce disease resistance against various pathogens by triggering ROS production. Foliar sprays with BABA triggered defense responses against the late blight pathogen Phytophthora infestans in potato by triggering H2 O2 production (Bengtsson et al. 2014a, b). BABA treatment has been shown to trigger ROS production and enhance disease resistance in grapevine against the downy mildew oomycete pathogen Plasmopara viticola (Dubreuil-Maurizi et al. 2010), in tomato against the bacterial pathogen Pseudomonas syringae pv. tomato (Baysal et al. 2006), and in Arabidopsis against the fungal pathogen Plectosphaerella cucumerina (Pastor et al. 2013). Spray application of BABA reduced the severity of the downy mildew disease caused by Peronospora belbahrii in basil. The plants treated with BABA showed significantly higher peroxidase activity than the non-treated control plants (Mersha et al. 2013).

3.8.2 BABA Primes NADPH Oxidase-Dependent ROS Production and Induces Disease Resistance BABA-induced resistance is mostly based on priming of defense responses rather than on the direct activation of these defense responses (Zimmerli et al. 2000, 2001; Hamiduzzaman et al. 2005; Ton et al. 2005; Dubreuil-Maurizi et al. 2010). BABA has been shown to prime an NADPH oxidase-dependent ROS production in grapevine (Dubreuil-Maurizi et al. 2010). NADPH oxidase is the key enzyme in ROS biosynthesis pathway (Lehtonen et al. 2012; O’Brein et al. 2012; Vidhyasekaran 2014). BABA primes RbohD gene, which encodes a NADPH oxidase potentially involved in ROS production in grapevine (Dubreuil-Maurizi et al. 2010). Water treatment or BABA treatment alone did not increase the transcription of RbohD gene in Arabidopsis. When the water-treated plants were inoculated with the fungal pathogen Plectosphaerella cucumerina, a slight increase in the expression of RbohD was observed.

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Relative expression of RBOHD gene

2.5 2 1.5 1 0.5 0 Water

Water+Pathogen

BABA

BABA+Pathogen

Fig. 3.13 BABA primes pathogen-induced transcription of RBOHD gene in Arabidopsis (Adapted from Pastor et al. 2013)

By contrast, very high increase in transcription of RbohD was observed in BABAtreated plants when they were challenge-inoculated with the pathogen (Fig. 3.13; Pastor et al. 2013). The results suggest that BABA primes RbohD gene expression and the gene encodes NADPH oxidase involved in ROS production. BABA itself does not induce ROS production in grapevine cells. In water- and BABA pretreated grapevine cells, the HAMP/endogenous elicitor oligogalacturonides (OG) treatment induced H2 O2 production; however, H2 O2 production was higher in BABA-pretreated cells. In water-pretreated cells, OG induced accumulation of RbohD gene transcripts within 30 min and in BABA-treated cells, RbohD transcript accumulation was higher than in water-treated cells. RbohD transcript accumulation was not observed in grapevine leaves after BABA treatment. From 3 days after inoculation with the downy mildew pathogen Plasmopara viticola, a strong H2 O2 production was observed in BABA-treated leaves; no H2 O2 production was observed in water-treated leaves. In response to the downy mildew pathogen P. viticola, a stronger ROS production was specifically observed in BABAtreated grapevine leaves. The NADPH oxidase inhibitor diphenylene iodonium (DPI) abolished this primed ROS production and reduced the BABA-induced resistance (Dubreuil-Maurizi et al. 2010). These studies suggest that BABA primes RbohD gene and the priming of NADPH oxidase-dependent ROS production is involved in BABA-triggered disease resistance.

3.8.3 ROS Homeostasis May Regulate Primed Immune Responses Reactive oxygen species possess a strong oxidizing potential that leads to damage to a variety of biological molecules (Halliwell 2006; Petrov and Van Breusegem 2012).

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ROS at high concentrations are toxic to plant cells leading to necrosis and cell death (Gechev and Hille 2005; de Pinto et al. 2006). During pathogenesis ROS levels can rise excessively, leading to an oxidative stress state (Apel and Hirt 2004). However, plants have evolved antioxidant system to control cellular ROS concentrations (Mittler et al. 2011). ROS at lower concentration act as signaling molecules triggering plant immune responses (Petrov and Van Breusegem 2012), while ROS at higher concentrations are toxic to plant cells. ROS homeostasis may play an important role in plant immune system. Interplay between ROS production enzymes (NADPH oxidase and cell wall peroxidase) and ROS scavenging enzymes (catalases, ascorbate peroxidase, glutathione peroxidase, superoxide dismutase) determine the ROS homeostasis. Both ROS production and activation of ROS-scavenging systems contribute to fine-tuning of ROS levels and their signaling properties (Torres et al. 2006). Foliar spray application of BABA on tomato leaves inoculated with the bacterial speck pathogen Pseudomonas syringae pv. tomato resulted in high H2 O2 generation and increased guaiacol peroxidase activity (Baysal et al. 2006). The same treatment also enhances the activity of ROS-degrading/scavenging enzymes. The activity of the ROS scavenging enzymes superoxide dismutase, ascorbate peroxidase and catalase also showed a significant increase in BABA-treated plants. These increases in both ROS production and scavenging enzymes activity induced by BABA coincided with the initiation of defense responses against the bacterial pathogen (Baysal et al. 2006). Fine tuning of ROS homeostasis has been shown to regulate primed immune responses against the necrotrophic fungal pathogen Plectosphaerella cucumerina in Arabidopsis (Pastor et al. 2013). Pretreatment of Arabidopsis with the BABA augmented H2 O2 production after inoculation with P. cucumerina. RBOHD (Respiratory burst oxidase D)/NADPH oxidase, the enzyme involved in ROS production, was found to be critical for BABA-induced resistance to P. cucmerina. BABA primed pathogen-induced transcription of the ROS-generating RBOHD gene. BABA suppressed APX1 (Ascorbate peroxidase 1) expression after infection with the pathogen. Conversely, GSH1 (γ-glutamylcysteine synthetase 1) was directly induced by BABA but was repressed following subsequent pathogen infection. However, ROS scavenging VTC1 (vitamin C defective 1) gene expression showed strongly augmented induction in BABA-treated plants (Pastor et al. 2013). BABA primed Arabidopsis plants showed a simultaneous increase in the expression of ROS-generating RBOHD and ROS-scavenging VTC1 genes (Pastor et al. 2013). The interplay between ROSgenerating and ROS-scavenging enzymes may be involved in homeostasis of ROS in plant cells (Vidhyasekaran 2014). The results suggest that fine tuning of ROS homeostasis regulates primed immune responses in Arabidopsis.

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3.9 Manipulation of ROS Signaling System Using Phosphorous Compounds for Crop Disease Management 3.9.1 Potassium Phosphonate Triggers ROS Signaling System-Mediated Plant Defense Responses Several phosphorous compounds have been developed as plant innate immunity activators. Phosphorous does not exist as a free element and occurs in combination with other elements, such as oxygen or hydrogen. It occurs in a fully oxidized form as phosphate anion (PO4 ) and as a reduced form of phosphate, phosphite. The conjugate acid of the phosphite anion is phosphorous acid (H3 PO3 ). The term phosphite is commonly referred to as the salts of phosphorous acid and the term phosphonate is used to mean phosphite ester containing a carbon-phosphorous (C-P) bond (Jackson et al. 2000; Thao and Yamakawa 2009). Phosphorous acid is a solid substance and when mixed with water, it forms a strong acid called phosphonic acid. This acid is too strong to be used on plants and must be combined with other chemicals to raise the pH of the solution. Phosphonic acid is neutralized with an alkali salt, particularly with potassium hydroxide (Thao and Yamakawa 2009). Phosphonates are specifically involved in inducing resistance against oomycete pathogens by triggering ROS production and downstream plant defense system (Daniel and Guest 2006). When Arabidopsis thaliana plants were treated with potassium phosphonate and challenge inoculated with the oomycete pathogen Phytophthora palmivora, rapid release of superoxide (O2 − ) was observed around the point of infection 6 h after inoculation (Fig. 3.14; Daniel and Guest 2006). Superoxide burst associated with the pathogen development could not be observed in untreated plants. Cells releasing superoxide subsequently underwent hypersensitive cell death (Daniel and Guest 2006). Superoxide release has been shown to be a key step in hypersensitive cell death in many plant-pathogen interactions (Doke 1983; Rabinowitch et al. 1987; Heath 2000). The superoxide anion is rapidly dismutated to the more stable H2 O2 by superoxide dismutase (SOD) (Vidhyasekaran 2014). The phosphonate-induced hypersensitive cell death in P. palmivora-inoculated Arabidopsis plants was accompanied by accumulation of phenolics. Accumulation of phenolic materials in A. thaliana began 6 h of inoculation in phosphonate-treated seedlings, the same time at which O2 − and H2 O2 was detected (Daniel and Guest 2006). Although the components required for hypersensitive cell death are pre-programmed as part of the Arabidopsis defense response, they are not elicited in response to challenge by P. palmivora in the absence of phosphonate (Daniel and Guest 2006). Phosphanate treatment induced resistance against P. palmivora in Arabidopsis (Daniel and Guest 2006). These results suggest that phosphanate triggers ROS-mediated defense responses. Phosphonate is a relatively inexpensive and environmentally innocuous, systemically mobile chemical (Guest and Grant 1991; Daniel et al. 2005; Daniel and Guest

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Arabidopsis plants

Potassium phosphonate application Pathogen inoculation

Superoxide

Superoxide dismutase

H2O2

Hypersensitive cell death

Activation of defense genes

Disease resistance Fig. 3.14 Phosphonate triggers superoxide release to activate plant defense responses (Adapted from Daniel and Guest 2006)

2006). Foliar sprays of phosphonic acid (partially neutralized with potassium hydroxide to pH 6.4) reduced infection of potato tubers by Phytophthora infestans (Cooke and Little 2001). It suggests that phosphonate may induce systemic resistance and/or translocation of the chemical from foliage to tuber in potato. Potassium phosphonate sprayed on foliage can move down to roots (Anil Kumar et al. 2009), suggesting that foliar application of potassium phosphonate can control soil-borne pathogens. Phosphonates are known to control plant diseases caused by oomycetes including Pythium, Phytophthora, and downy mildew pathogens (Vawdrey et al. 2004; Cook et al. 2009). Efficacy of potassium phosphonate in controlling root rot of papaya

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caused by Phytophthora palmivora has been demonstrated in field trials conducted in Australia. Foliar sprays of potassium phosphonate (10 g/l) applied fortnightly reduced the incidence of root rot by 47% (Vawdrey et al. 2004). Phosphonate compounds applied by trunk injections, soil drenches, topical applications, and foliar sprays efficiently controlled sudden oak death caused by Phytophthora ramorum in oak (Quercus agrifolia) and tanoak (Lithocarpus densiflora) (Garbelotto and Schmidt 2009). Several commercial phosphanate formulations have been developed. Fosetyl-Al is manufactured by converting phosphonic acid to ethyl-phosphonate by adding ethanol to phosphonic acid. Aluminium ions are added during the manufacturing process to neutralize the ethyl-phosphonate ions and the resulting product is fosetyl-Al. This is the active ingredient in Aliette. Aliette (aluminium tris-o-ethyl phosphonate) is a substituted phosphonate formulation. Fosetyl-Al is broken down to phosphonate in the plant (Grant et al. 1990). Another product containing fosetyl-Al is Chipco Signature, which contains a blue pigment besides fosetyl-Al. Phytogard is a formulation containing 58% potassium phosphonate (K2 HPO3 ) (Becot et al. 2000). AG3 (Calrus 150, liquid formulation; 10.45% a.i. phosphorous acid and copper sulfate with citrate as a chelating agent) is another phosphonate formulation (Abbasi and Lazarovits 2006). The phosphonate formulation Aliette (at 2000 ppm a.i.) delayed the appearance of necrotic local lesions induced by Alfalfa mosaic virus (AMV) (Abu-Jawdah and Kummert 2008). It induced resistance against the fireblight bacterial pathogen Erwinia amylovora in the ornamental pear (Pyrus kawakami) (Elam and Holmes 1991) and also against blast of dormant flower buds of pear caused by Pseudomonas syringae pv. syringae (Montesinos and Vilardell 2001). Another potassium phosphonate formulation, Phytogard, induced systemic resistance against downy mildew of cauliflower (Brassica oleracea var. botrytis) caused by Peronospora parasitica. When it was applied on roots of 30-day-old cauliflower plants, all leaf stages were completely protected against P. parasitica (Becot et al. 2000). It provided complete protection of seedlings, when sprayed at 7 ml/l of water. The induced resistance persisted at least for 15 days (Becot et al. 2000). Phytogard induced resistance against downy mildew (Bremia lactucae) in lettuce. Phytogard sprayed at 40.6 ppm provided complete protection against the pathogen and the induced systemic resistance (ISR) lasted for at least 15 days (Pajot et al. 2001). Tree Doc is another phosphanate formulation. Avocado trees were injected with a phosphonate formulation, Tree Doc has been shown to control avocado tree root rot caused by Armillaria sp. in New Zealand (Sale 1999). Tree Doc injected at 30% was more effective than that injected at lower concentrations (Sale 1999). Another phosphonate formulation, AG3 (Calirus) controls Pythium damping-off of cucumber (Abbasi and Lazarovits 2005, 2006). The phosphonate seed soak provided more than 80% control of damping-off of cucumber. Post-planting drench with the phophonate was also effective in reducing the damping-off disease incidence; however, seed soak treatment was more effective than post-planting drench (Abbasi and Lazarovits 2006).

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3.9.2 K2 HPO4 Triggers ROS Signaling in Plant Immune System Potassium dihydrogen phosphate induced systemic resistance against the powdery mildew pathogen Sphaerotheca fuliginea in cucumber seedlings (Reuveni et al. 2000). A local spray application of dipotassium hydrogen phosphate (K2 HPO4 ) was effective in inducing a high level of systemic protection in cucumber plants against anthracnose caused by Colletotrichum lagenarium (Orober et al. 2002). It induced a rapid generation of superoxide and hydrogen peroxide. It also induced a local and systemic increase in free and conjugated salicylic acid levels (Orober et al. 2002). None of these responses was triggered by application of BTH, which nevertheless was effective in inducing systemic resistance in cucumber against anthracnose. It suggests that mechanisms of induction of resistance by K2 HPO4 and BTH may be different from each other (Orober et al. 2002). Potassium dihydrogen phosphate (trade names: Nutrol, eKsPunge. Vital) induces resistance against several pathogens (Reuveni et al. 2000). When it was sprayed at 1% concentration plus Tween20, severity of powdery mildew (Uncinula necator) in grapevine was reduced by 76–99% in different trials. Sporulation was reduced 50 to 95% (Carroll and Wilcox 2001). In a two-year trial conducted in Italy, potassium dihydrogen phosphate gave acceptable powdery mildew control in grapevine, comparable to standard fungicides (Egger and D’Arcangelo 2000). It also controlled powdery mildew (Oidium mangiferae) in mango (Oosthuyse 1998). Its efficacy increased when it was applied as a mixture with fungicides such as triadimenol (Oosthuyse 1998).

3.10 Reactive Oxygen Species Generators as Plant Innate Immunity System Activators for Crop Disease Management Oxycom™ is a commercially available chemical containing reactive oxygen species. It acts as a plant innate immunity activator (Kim et al. 2001). Applications of Oxycom triggered plant immune system downstream of ROS. It enhanced expression from PR-1a promoter and production of the PR-1 protein in tobacco. Enhanced activity occurred systemically both from aerial applications of the ROS generator Oxycom to single leaves and from root drenches. Root application strongly promoted expression of the PR-1a promoter in leaf veins of sprayed seedlings (Blee et al. 2004). Oxycom treatment induces resistance against the bacterial pathogen Pseudomonas syringae pv. tabaci in tobacco (Yang et al. 2002; Blee et al. 2004). Symptoms were reduced and bacterial multiplication was inhibited in leaves pretreated with Oxycom in comparison to the levels in leaves treated with water. Oxycom-treatment enhanced the accumulation of PR-1 protein occurring after challenge by the bacterial pathogen. It induced greater accumulations of PR-1a, PR-1g and PR-3a transcripts.

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It also caused rapid phosphorylation of mitogen-activated protein kinase (MAPK), which is also phosphorylated by salicylic acid (Yang et al. 2002). Collectively these results suggest that Oxycom activates the SA-activated MAPK pathway in downstream ROS and induces expression of several PR proteins conferring resistance against pathogens. Oxycom has been shown to be effective in controlling oomycetes (Pythium and downy mildew) and fungal pathogens (powdery mildews) in various plants (Kim et al. 2001).

3.11 Manipulation of ROS and Redox Signaling System Using Microbes to Trigger Immune Responses for Crop Disease Management 3.11.1 Pseudomonas aeruginosa Induces ISR by Triggering ROS Signaling System Several bacterial and fungal biocontrol agents have been shown to induce systemic resistance (ISR) against several plant pathogens in various crop plants (Vidhyasekaran 2002, 2004, 2007; Bargabus et al. 2003, 2004; De Vleesschauwer et al. 2006, 2008, 2009; Ahn et al. 2007; Tran et al. 2007; Perazzoli et al. 2011; Verhagen et al. 2011). Some of the rhizobacteria activate the plant innate immune system by triggering the ROS signaling system. Pseudomonas aeruginosa strain 7NSK2 is known to activate the immune system in rice. Pyocyanin, a phenazine antibiotic, has been identified as an elicitor secreted by the rhizobacterium P. aeruginosa strain 7NSK2 triggering induced systemic resistance against the rice blast pathogen Magnaporthe oryzae. Roots of rice seedlings treated with pyocyanin showed strong induction of ROS (De Vleesschauwer et al. 2006). Changes in total superoxide dismutase activity were concomitant with the biphasic generation pattern of H2 O2 , suggesting that pyocyanin-induced H2 O2 accumulates sequentially from superoxide as the primary origin. The first phase of H2 O2 accumulation coincided with declined activities of catalase and guaiacol peroxidase. During the second phase of generation of H2 O2 , both ascorbate and guaiacol peroxidase activity progressively increased (De Vleesschauwer et al. 2006). Co-application of the H2 O2 quenching agent sodium ascorbate and pyocyanin solution attenuated the pyocyanin-triggered resistance to the rice blast pathogen Magnaporthe grisea (De Vleesschauwer et al. 2006). No significant reduction in blast disease development was observed in rice plants when the rice roots were treated with the pyocyanin mutant P. aeruginosa 7NSK2-phzM, which doesn’t produce pyocyanin (Fig. 3.15; De Vleesschauwer et al. 2006). These results strongly suggest that ROS generated by pyocyanin is involved in P. aeruginosa 7NSK2-induced ISR in rice plants. P. aeruginosa 7NSK2 is a plant growth-promoting rhizobacterium (PGPR). It has been reported that it induces ISR against several pathogens in tomato, tobacco, and bean, besides rice plants (De Meyer

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120 100 80

Relative M. oryzae infection (% of control)

60 40 20 0

Control

PyocyaninPyocyanin producing wild nonpoducing P. P. aeruginosa aeruginosa strain strain

Fig. 3.15 Pyocyanin produced by Pseudomonas aeruginosa strain triggers ROS signaling to activate defense responses against the rice blast pathogen Magnaporthe oryzae (Adapted from De Vleesschauwer et al. 2006)

and Hofte ¨ 1997; De Meyer et al. 1999a, b; Audenaert et al. 2002; Bigirimana and Höfte 2002; De Vleesschauwer et al. 2006).

3.11.2 Pseudomonas fluorescens WCS374r Induces ROS-Mediated Disease Resistance The rhizobacterium Pseudomonas fluorescens WCS374r, which has been found to be potential inducer of plant innate immune system, was isolated from the rhizosphere of potato (Leeman et al. 1995b, 1996). Application of P. fluorescens WCS374r to soil induced resistance in rice leaves against the blast pathogen Magnaporthe grisea. P. fluorescens WCS374r effectively controlled rice blast disease when it was applied as root treatment (Fig. 3.16; De Vleesschauwer et al. 2008). Plants colonized by the WCS374r strain showed a 47% reduction in lesion number (De Vleesschauwer et al. 2008). Pseudobactin, a siderophore isolated from P. fluorescens WCS374r induced resistance against the rice blast pathogen M. oryzae and pseudobactin-mediated resistance involved a timely, highly localized, and well-restricted production of H2 O2 in the epidermis of rice leaves. Pseudobactin-induced H2 O2 -mediated resistance against M. oryzae appears to be associated with priming for accelerated cell wall fortification. H2 O2 is used as a substrate for peroxidase-dependent cross-linking of cell wall polymers. Cell wall modification was more abundant and appeared earlier in pseudobactin-treated plants after inoculation with the pathogen than in the control plants. Increased protein cross-linking was also detected in pseudobactinsupplied cells, when challenge inoculated with M. oryzae. Pseudobactin also primes rice plants for augmented deposition of phenolic compounds at sites of attempted

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M. oryzae relaƟve infecƟon %

60 40 20 0 Control

P. fluorescens WCS3742

Fig. 3.16 Pseudomonas fluorescens WCS3742 induces ROS-mediated resistance against the rice blast pathogen Magnaporthe oryzae (Adapted from De Vleesschauwer et al. 2008)

pathogen entry. The cell wall fortification with phenolic deposits may prevent the entry of the pathogen into host cell (De Vleesschauwer et al. 2008). P. fluorescens WCS374 has been shown to suppress Fusarium wilt of radish caused by Fusarium oxysporum f. sp. raphani (Leeman et al. 1995b, 1996). The P. fluorescens strain WCS374 induced systemic resistance against the radish Fusarium wilt (Leeman et al. 1995a). Seed treatment with the strain reduced the Fusarium wilt incidence by about 42% and increased the yield by about 45% when compared with untreated control in radish crop (Hoffland et al. 1995; Leeman et al. 1995a). It has also been found useful in management of the bacterial wilt disease caused by Ralstonia solanacearum in Eucalyptus urophylla (Ran et al. 2005). These studies suggest that P. fluorescens WCS374 is a potential tool to trigger ROS signaling system and confer resistance against pathogens.

3.11.3 Serratia plymuthica Primes Plants for Enhanced Attacker-Induced Accumulation of ROS and Triggers ISR ROS can play a dual role in host plant’s defense response, acting as key players in resistance to biotrophic pathogens on the one hand (Levine et al. 1994; Van Breusegem and Dat 2006; De Vleesschauwer et al. 2009), while weakening necrotroph resistance by assisting pathogen-induced host cell death on the other (Govrin and Levine 2000; Glazebrook 2005; Govrin et al. 2006; De Vleesschauwer et al. 2009). ROS signaling system triggers cell death, which may induce resistance to biotrophic pathogens and induce susceptibility to necrotrophic pathogens. Root treatment with the rhizobacterial strain, Serratia plymuthica ICI270, primes rice leaves for enhanced attacker-induced accumulation of ROS and phenolic compounds in and

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near epidermal cells (De Vleesschauwer et al. 2009). S. plymuthica IC1270 induced accumulation of ROS in rice leaves challenge-inoculated with pathogens and induced systemic resistance to the hemibiotrophic pathogen M. oryzae and susceptibility to the necrotrophic pathogens Rhizoctonia solani and Cochliobolus miyabeanus (De Vleesschauwer et al. 2009).

3.11.4 Bacillus mycoides Elicits Systemic Induced Resistance by Triggering ROS Production Bacillus mycoides Bac J isolated from sugar beet leaves has been identified as a potential biocontrol agent, which induces systemic resistance in sugar beet against Cercospora beticola (Bargabus et al. 2001, 2002, 2003). The phyllosphere microorganism elicited an oxidative burst in sugar beet similar in timing to that elicited during the incompatible Erwinia carotovora pv. betavasculorum interactions (Bargabus et al. 2003). The oxidative burst was seen only following live B. mycoides Bac J cell treatment (Bargabus et al. 2003), a requirement for effective disease control (Bargabus et al. 2002). Furthermore, the Bacillus sp. isolate incapable of inducing systemic resistance failed to elicit the characteristic biphasic H2 O2 production curve induced by B. mycoides Bac J isolate (Bargabus et al. 2003). These results suggest that B. mycoides Bac J induces ROS-mediated induced systemic resistance in sugar beet. B. mycoides may be another potential biocontrol agent, which can be exploited for management of various diseases.

3.11.5 Bacillus pumilus Triggers ROS-Mediated Induced Systemic Resistance Besides Bacillus mycoides Bac J, two Bacillus pumilus isolates, 203-6 and 203-7, have been shown to trigger systemic acquired resistance against Cercospora beticola in sugar beet (Bargabus et al. 2004). Induction of systemic resistance was preceded by biphasic hydrogen peroxide production, suggesting an important role of ROS in inducing defense responses. B. pumilus isolates 203-6 and 203-7 reduced Cercospora leaf spot symptoms by approximately 70%, even when spatially separated from the causal agent, Cercospora beticola. The level of control was similar to B. mycoides isolate Bac J and acibenzolar-S-methyl (Bargabus et al. 2004). These results suggest that B. pumilus can be developed as an additional tool for crop disease management.

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3.12 Manipulation of ROS Signaling by Silicon to Activate Plant Innate Immune Responses Silicon is another potential tool to enhance defense responses by activating ROS signaling system. Silicon application significantly reduced the blast disease incidence in rice (Fig. 3.17; Sun et al. 2010). Rice plants applied with silicon as a single dose immediately after Magnaporthe oryzae inoculation exhibited the same high protection against the blast disease as plants treated continuously with silicon for the whole growth period. Silicon treatment significantly altered the activity of lipoxygenase in rice plants (Sun et al. 2010). Lipoxygenase (LOX) catalyses the direct oxygenation of polyunsaturated fatty acids (Saniewski 1979) and LOX activity produces O2 − (Lynch and Thompson 1984; Thompson et al. 1987). O2 − arises as a by-product from many oxidoreductase enzymes when electrons leak from the reaction and reduce molecular oxygen (Halliwell and Gutteridge 1989). Silicon induced a rapid transient burst of H2 O2 at 24 h after inoculation with the pathogen M. oryzae. The addition of Si to rice plants significantly altered the activities of lipoxygenase and catalase and the concentration of malondialdehyde (indicative of lipid peroxidation) in rice plants (Sun et al. 2010). These responses were found to be linked to host defense responses such as lignin production, oxidative cross-linking in the cell wall and the hypersensitive responses (Fig. 3.18; Sun et al. 2010). Silicon treatment induced lipid peroxidation in rice plants (Sun et al. 2010). Lipid peroxidation is a reaction of lipid with molecular oxygen (Yin et al. 2011). Lipid peroxidation is a process in which free radicals remove electrons from lipids, producing reactive intermediates (Kiang et al. 2012). Molecular oxygen reacts with unstable lipid radical to produce a lipid peroxy radical (Kiang et al. 2012). The formation of fatty acid hydroperoxides is a reaction catalyzed by lipoxygenase (LOX) enzymes 70 60 50

Disease severity (%)

40 30 20 10 0 Control

Silicon treatment

Fig. 3.17 Silicon triggers H2 O2 -mediated induced resistance in rice plants against Magnaporthe oryzae Adapted from Sun et al. (2010)

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Lipids

Lipase Silicon Linolenic acid Lipoxygenase Molecular oxygen

13-Hydroperoxy octadecatrienoic acid+singlet oxygen

Superoxide Superoxide dismutase Triggers Silicon

H2O2

Polyunsaturated fatty acids

Lipid peroxidation

Silicon

Malondialdehyde (MDA)

Lignification

Fig. 3.18 Silicon application triggers lipoxygenase activity, ROS production and lipid peroxidation to enhance defense responses (Adapted from Croft et al. 1990; Sun et al. 2010; Chen et al. 2013)

(Bertoni 2012). Lipid peroxidation induced by lipoxygenase activity may lead to production of ROS (Croft et al. 1990). Lipoxygenase catalyzes the direct oxygenation of polyunsaturated fatty acids and produces O2 − (Thompson et al. 1987). In turn ROS may initiate enzyme-independent lipid peroxidation (Croft et al. 1990). Malondialdehyde (MDA) is a decomposition end product of polyunsaturated fatty

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acids (Mittler 2002). Silicon treatment induces formation of MDA (Sun et al. 2010). Activation of O2 − and H2 O2 production and increased lipid peroxidation resulting in accumulation of MDA are known to trigger increased lignification (Sun et al. 2010; Chen et al. 2013). In rice plants, the lignin content of leaf tissues increases with silicon treatment (Cai et al. 2008). These results suggest that silicon triggers ROS and lipid peroxidation involved in the ROS signaling system activating defense responses. Several silicon-based formulations are available to trigger immune responses in plants. These include Silica Plus™ (Grose ‘n’ Grows P/L QLD)) and Photo-Finish™ (Nutri-tech Solutions P/L., QLD, and Kasil 2040 (PQ Australia P/L Vic.). Monosilicic acid is the form of silicon available to the plant and it induces PR proteins (Dann and Muir 2002). Si application resulted in accumulation of monosilicic acid in leaves of pea plants. Accumulation of monosilicic acid resulted in early activation of host plant’s innate immunity system. It resulted in suppression of lesion development induced by the fungal pathogen Mycosphaerella pinodes in pea (Dann and Muir 2002). Silicon application significantly reduced bacterial wilt incidence caused by Ralstonia solanacearum in tomato (Dannon and Wydra 2004). Silicon application increases rice resistance to blast on both partially resistant and susceptible cultivars (Seebold et al. 2001), sheath blight caused by Rhizoctonia solani (Rodrigues et al. 2003) and brown spot caused by Cochliobolus miyabeanus in rice (Datnoff et al. 1992). Rice plants treated with silicon exhibited an enhanced resistance against infection by M. oryzae (Rodrigues et al. 2004, 2005). Silicon is known to induce host defense mechanisms (Dannon and Wydra 2004). Silicon induces defense responses that are functionally similar to systemic acquired resistance. Silicon increased resistance to powdery mildew (Podosphaera xanthii) in cucumber (Fawe et al. 1998). Silicon treatment induced resistance against wheat powdery mildew caused by Blumeria graminis f. sp. tritici (Rémus-Borel et al. 2005). Exogenous application of silicon in the form of sodium metasilicate reduced fruit decay caused by Penicillium expansum and Monilinia fructicola in sweet cherry (Qin and Tian 2005). Sodium silicate reduced postharvest decay on Hami melons caused by Alternaria alternata, Fusarium spp., and Trichothecium roseum (Bi et al. 2006).

3.13 Bioengineering Cysteine-Rich Receptor-Like Kinase (CRK) Genes to Activate ROS-Modulated Plant Immune Responses for Disease Management Receptor-like kinases (RLKs) play important role in signal transduction in plants (Bourdais et al. 2015). The plant cell surface RLKs link perception of external stimuli and downstream signal transduction to trigger intracellular responses (Yeh et al. 2015). The RLKs contain an extracellular signal-sensing domain connected by a single transmembrane domain to an intracellular protein kinase domain (Shiu and

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Bleecker 2003). RLKs consist of a N-terminal receptor domain in the extracellular region, a transmembrane domain, and a C-terminal intracellular protein kinase domain (De Smet et al. 2009). RLKs are classified according to their extracellular domains (Shiu and Bleecker 2003). Cysteine-rich receptor-like kinases (CRKs) are one of the largest groups of RLKs. The extracellular domain of CRKs encompasses two copies of the DUF26 (domain of unknown function 26) domain, which contains three cysteine residues in a conserved configuration and is a target for redox modification (Bourdais et al. 2015). The presence and spacing of the conserved cysteines in the DUF26 domain suggest that CRKs are connected to redox and reactive oxygen species (ROS) signaling (Chen 2001; Wrzaczek et al. 2010, 2013). Several CRKs have been shown to play important role in triggering plant immune system (Acharya et al. 2007). The wheat CRK TaCRK1 is more expressed in wheat varieties resistant to Rhizoctonia cerealis (Yang et al. 2013). The CRKs appear to trigger the plant immune responses by activating ROS signaling system (Bourdais et al. 2015; Yeh et al. 2015). Transgenic Arabidopsis plants overexpressing the Arabidopsis CRK4, CRK6, and CRK36 genes were developed. ROS production was found to be increased in the CRK4 (Fig. 3.19; Yeh et al. 2015), CRK6, and CRK36 overexpressing plants after treatment with the pathogenassociated molecular pattern (PAMP) flg22. Overexpression of CRK4, CRK6, and CRK36 enhanced the production of flg22-triggered ROS production. No constitutive ROS production was observed in mock-treated plants. Flg22 treatment alone induced ROS production in the wild-type plants, but ROS production was further enhanced in the transgenic plants treated with the PAMP (Yeh et al. 2015). The results show priming of ROS accumulation upon PAMP-triggered immunity (PTI) elicitation in CRK4, CRK6, and CRK36 overexpressing lines. Arabidopsis lines overexpressing CRK4 (Fig. 3.20), CRK6, and CRK36 were found to be highly resistant to the bacterial pathogen Pseudomonas syringae pv. tomato DC 3000 showing reduced bacterial titer (Yeh et al. 2015). The disease symptom development was also reduced in the transgenic plants (Yeh et al. 2015). 14000 12000 10000

Reactive oxygen 8000 species (RLU) 6000 4000 2000 0 CRK4 Col-O wild-type overexpressing plants (after line (after flg22 flg22 treatment) treatment)

Fig. 3.19 Priming of ROS accumulation upon flg22 treatment in Arabidopsis lines overexpressing CRK4 gene (Adapted from Yeh et al. 2015)

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Bacterial number (log CFU/cm2)

4 3 2 1 0 Col-O (wild-type Transgenic CRK4 plants) overexpressing line

Fig. 3.20 Arabidopsis plants overexpressing CRK4 gene show enhanced resistance to Pseudomonas syringae pv. tomato DC3000. (Adapted from Yeh et al. 2015)

These studies reveal the potential of CRKs in developing disease resistant plants by enhancing ROS production.

3.14 Bioengineering Lectin Receptor Kinase (LecRK) Genes to Activate ROS-Modulated Plant Immune Responses for Disease Management Lectin receptor kinases such as L-type lectin receptor kinases (LecRKs) play a critical role in PAMP-triggered innate immunity (PTI) (Singh and Zimmerli 2013). LecRKs possess an extracellular lectin domain, a transmembrane domain and an intracellular kinase domain (Bouwmeester and Govers 2009). They are associated with the pattern recognition pattern (PRR) and form a component in the PAMPPRR signaling complex (Huang et al. 2014). LecRKs are known to function in plant innate immunity (Bouwmeester and Govers 2009; Bouwmeester et al. 2011; DesclosTheveniau et al. 2012; Singh et al. 2012a, b; Singh and Zimmerli 2013; Huang et al. 2014). AtLecRK-1.9 has been shown to be essential for triggering resistance against pathogens (Bouwmeester et al. 2011). AtLecRK-V.5 triggers ROS biosynthesis and negatively regulates immune responses (Arnaud et al. 2012; Desclos-Theveniau et al. 2012). LecRK-VI.2 modulates bacterium-mediated PTI (Singh et al. 2012a). LecRKs have been exploited to develop disease-resistant plants. Transgenic Arabidopsis plants overexpressing LecRK-VI.2 showed enhanced resistance against Pseudomonas syringae and Pectobacterium carotovorum bacteria (Singh et al. 2012a). Expression of the Arabidopsis LecRK-1.9 gene in potato and Nicotiana benthamiana results in significantly enhanced resistance to the late blight pathogen

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Phytophthora infestans (Bouwmeester et al. 2014). Overexpression of LecRK1.9 gene in Arabidopsis has been shown to lead to enhanced resistance to Phytophthora brassicae (Bouwmeester et al. 2011). Arabidopsis LecRK-VI.2 was transferred to Nicotiana benthamiana and the transgenic N. benthamiana plants expressing Arabidopsis LecRK-VI.2 showed increased production of ROS when treated with the PAMP flg22 (Fig. 3.21; Huang et al. 2014). Transient production of H2 O2 is rapidly induced upon the PAMP treatment in both wild-type and transgenic plants expressing LecRK-VI.2. However, the transgenic N. benthamiana plants produced significantly higher levels of ROS within 30 min after the PAMP treatment than wild-type plants. ROS production in the transgenic N. benthamiana plants ectopically expressing LecRK-VI.2 without the PAMP flg22 treatment the production of ROS (mock controls) was only at the level observed in the wild-type plants (Huang et al. 2014). The results suggest that expression of LecRKVI.2 in N. benthamiana primes ROS production induced by the PAMP and triggers defense responses against bacterial pathogens. The transgenic N. benthamiana plants expressing the Arabidopsis LecRK-VI.2 showed enhanced resistance against Pseudomonas syringae pv. tabaci (Fig. 3.22; Huang et al. 2014). The transgenic plants also showed resistance against a broad range of bacterial pathogens including Pseudomonas syringae pv. syringae and Pectobacterium carotovorum pv. carotovorum, besides P. syringae pv. tabaci (Huang et al. 2014). These studies suggest that the LecRK gene is a potential tool to develop disease resistant plants by modulating ROS signaling system. 140000 120000 100000

Reac ve oxygen species (RLU)

80000 60000 40000 20000 0 Wild-type plants Transgenic plants aŌer flg22 expressing LecRKtreatment Vi.2 gene aŌer flg22 treatment

Fig. 3.21 Priming of ROS production in transgenic Nicotiana benthamiana plants expressing LecRKVI.2 gene after the PAMP flg22 treatment (Adapted from Huang et al. 2014)

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Bacterial popula on (log cfu/cm2)

4 3 2 1 0 Wild-type plants

Transgenic plants overexpressing LecRKVI.2 gene

Fig. 3.22 Transgenic Nicotiana benthamiana plants overexpressing LecRK-VI.2 gene against Pseudomonas syringae pv. tabaci. (Adapted from Huang et al. 2014)

3.15 Engineering Peroxidase Gene to Activate ROS-Mediated Plant Immune Responses for Crop Disease Management NADPH oxidases are the key enzymes in production of ROS in plant cells (Love et al. 2005). Besides the NADPH oxidases, peroxidases have been shown as alternative producers of ROS (Bindschedler et al. 2006; Choi et al. 2007). Peroxidases in the cell wall can generate apoplastic H2 O2 at neutral to basic pH in the presence of reductants in plant cells (Bolwell et al. 1998). It is possible to generate transgenic plants overexpressing peroxidase gene to overproduce peroxidase resulting in enhanced ROS accumulation. The ROS accumulation would trigger the defense-related genes. Transgenic Arabidopsis plants overexpressing the pepper peroxidase 2 (CaPO2) gene showed enhanced resistance against Pseudomonas syringae pv. tomato infection (Fig. 3.23; Choi et al. 2007). Overexpression of CaPO2 in Arabidopsis increases H2 O2 generation and PR gene induction in response to P. syringae pv. tomato infection (Choi et al. 2007). The Arabidopsis PR genes were not expressed in healthy plants but induced in plants infected by pathogens. In wild-type plants, PR-1, and PR-5 were slightly induced by mock and P. syringae pv. tomato. However, the transgenic Arabidopsis overexpressing CaPO2 exhibited a rapid and significantly enhanced induction of NPR1, PR-1, and PR-5 after mock and the bacterial infection (Choi et al. 2007). This result suggests that ectopic expression of the CaPO2 gene in Arabidopsis triggers the ROS-mediated SA-dependent defense pathway and induces resistance against bacterial pathogen. It appears that development of transgenic crop plants overexpressig peroxidase gene may be a potential technology to manage crop diseases.

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7 6 5

Bacterial growth (log cfu/cm2)

4 3 2 1 0 Wild-type plants

Transgenic plants overexpressing CaPO2 gene

Fig. 3.23 Transgenic Arabidopsis plants over-expressing CaPO2 gene show enhanced resistance to Pseudomonas syringae pv. tomato DC3000 (Adapted from Choi et al. 2007)

3.16 Bioengineering Superoxide Dismutase to Activate ROS-Mediated Immune Signaling for Disease Management Superoxide dismutase (SOD) is a key enzyme involved in generation of H2 O2 in plant tissues (Rietz et al. 2012). Lipoxygenase catalyzes the direct oxygenation of polyunsaturated fatty acids and produces superoxide (O2 − ) (Thompson et al. 1987). O2 − is the first ROS induced by PAMP treatment/pathogen inoculation (Haga et al. 1995; Faize et al. 2004; Deepak et al. 2006). The superoxide is only short lived (Sagi and Fluhr 2006). The half life of O2 − is less than a second and is rapidly dismutated by SOD to H2 O2 , which is relatively stable (Grant and Loake 2000; Tertivanidis et al. 2004). H2 O2 plays an important role in activating SA (León et al. 1995), JA (Vandenabeele et al. 2003), and ethylene (Desikan et al. 2005) signaling systems triggering defense responses. SOD has been shown to be involved in triggering disease resistance responses in different plants (Tertivanidis et al. 2004; Banerjee et al. 2010; Banerjee and Maiti 2010; Ehsani-Moghaddam et al. 2008; Guevara-Olvera et al. 2012; Rietz et al. 2012). Germin is the protein, which accumulates in germinating embryos of wheat and barley (Lane et al. 1992, 1993). The germin shows oxalate oxidase activity, which is involved in ROS biosynthesis (Dumas et al. 1993; Whittaker and Whittaker 2002). Several germin-like proteins (GLPs) have been detected in various plants (Gucciardo et al. 2007; Manosalva et al. 2009; Schweizer et al. 1999; Lou and Baldwin 2006; Himmelbach et al. 2010; Knecht et al. 2010; LeÐn-Galván et al. 2011; GuevaraOlvera et al. 2012; Rietz et al. 2012). Many GLPs have been shown to possess superoxide dismutase, which converts superoxide to H2 O2 (Gucciardo et al. 2007; Banerjee et al. 2010; Banerjee and Maiti 2010). The germin-like proteins GER4 and GER5 isolated from barley show superoxide dismutase activity, which leads to the

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generation of H2 O2 (Druka et al. 2002; Zimmermann et al. 2006; Himmelbach et al. 2010). The germin-like protein GLP4 from barley exhibits superoxide dismutase activity and it has been shown to be involved in conferring disease resistance in wheat and barley (Christensen et al. 2004). The coding sequence of the germin-like protein PsGER1 isolated from pea when transiently expressed in tobacco leaves gave a protein with superoxide dismutase activity (Gucciardo et al. 2007). Some germin-like protein genes have been exploited to modulate ROS signaling system for developing disease-resistant plants. Geminiviruses are plant DNA viruses causing severe diseases in many crop plants. The germin-like protein gene, CchGLP has been cloned from Capsicum chinense and the transgenic tobacco plants expressing the gene from pepper showed enhanced resistance to the geminivirus infection (Guevara-Olvera et al. 2012). Arabidopsis thaliana transgenic plants expressing the germin-like protein gene BnGLP12 isolated from Brassica napus showed increased SOD activity (Fig. 3.24; Rietz et al. 2012) and the transgenic plants showed enhanced resistance against Sclerotinia sclerotiorum (Fig 3.25; Rietz et al. 2012). These results Membrane lipids

Lipoxygenase Expression of BnGLP12 gene from Brassica napus in transgenic Arabidopsis plants

Superoxide

Triggers overexpression

Superoxide dismutase

H2O2

Enhanced plant immune responses

Disease resistance Fig. 3.24 Transgenic Arabidopsis plants expressing BnGLP12 gene from Brassica napus show enhanced resistance responses by triggering superoxide dismutase-modulated H2 O2 production (Adapted from Rietz et al. 2012)

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300 250 200

Disease index 150 100 50 0 Wild-type plants

Transgenic plants expressing BnGLP12 gene

Fig. 3.25 Transgenic Arabidopsis plants expressing BnGLP12 gene show enhanced resistance against Sclerotinia sclerotiorum (Adapted from Rietz et al. 2012)

suggest that germin-like protein genes with SOD activity are potential tools for developing disease-resistant plants. Three different classes of SODs have been recognized in plants, based on their metal cofactor. Plants generally contain Cu/ZnSOD in the cytosol, FeSOD and/or Cu/ZnSOD in the chloroplasts, and MnSOD in the mitochondria (Baum and Scandalios 1979). Cytoplasmic Cu/ZnSOD (cytCu/ZnSOD) and chloroplast Cu/ZnSOD (chlCu/ZnSOD) genes have been cloned from tomato and transgenic sugarbeet plants expressing these tomato genes have been developed (Tertivanidis et al. 2004). These transgenic plants showed enhanced resistance against the sugarbeet leaf spot pathogen Cercospora beticola. SOD proteins encoded by genes originated from tomato were found to be targeted to the cytoplasm and the chloroplast in sugarbeet. No phenotypic differences were observed between transgenic and non-transgenic plants at any developmental stage (Tertivanidis et al. 2004). These studies suggest that SOD genes can be exploited to enhance the plant innate immunity potential to resist the pathogen attack.

3.17 Engineering Glucose Oxidase Gene to Trigger ROS Production for Management of Crop Diseases Fungal glucose oxidase gene has been used to develop disease-resistant plants (Frederick et al. 1990 Wu et al. 1995; Felcher et al. 2003; Maruthasalam et al. 2010). Glucose oxidase gene encodes β-D-glucose:oxygen 1-oxidoreductase which catalyzes the oxidation of β-D-glucose by molecular oxygen, yielding gluconic acid and H2 O2 (Wu et al. 1995). Oxidation of β-D-glucose by glucose oxidase leads to the accumulation of H2 O2 (Felcher et al. 2003; Maruthasalam et al. 2010). A number of fungi

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and bacteria produce glucose oxidase, but glucose oxidase has not been detected in plants and animals (Frederick et al. 1990). Wu et al. (1995) developed transgenic potato plants expressing the gene encoding glucose oxidase isolated from the genome of the fungus Aspergillus niger. The transgene was found to be expressed in both leaf and tuber tissues. The glucose oxidase in the transgenic potato plants was found to be secreted into the apoplast. Expression of the fungal glucose oxidase gene was found to lead to elevated production of H2 O2 in the transgenic potato plants (Fig. 3.26; Wu et al. 1995). The increased level of H2 O2 in the transgenic potato plants resulted in increased resistance against the late blight oomycete pathogen Phytophthora infestans (Wu et al. 1995). The transgenic potato plants expressing the fungal glucose oxidase gene also showed strong resistance against the soft rot bacterial pathogen Pectobacterium carotovorum (formerly known as Erwinia carotovora subsp. carotovora). Nearly complete control of soft rot was observed in the transgenic potato tubers, while tubers of untransformed potato showed severe tissue maceration. The amount of H2 O2 in tuber tissues of transgenic lines was two-to-threefold higher than in control lines soft rot resistance in the transgenic tubers was abolished by the addition of catalase. These results suggest that soft rot resistance Lee et al. (2002) in the transgenic potato tubers expressing glucose oxidase is due to accumulation of H2 O2 in the tubers. The transgenic plants were also found to be phenotypically indistinguishable from the nontransgenic plants (Wu et al. 1995). While Wu et al. (1995) used 35S-promoter of figwort mosaic virus to develop disease-resistant transgenic plants expressing fungal glucose oxidase, Zhen et al. (2000) amplified the coding region of the glucose oxidase gene from Aspergillus niger via PCR and fused to the pathogen-inducible promoter, Prp1-1. The chimeric gene was cloned into a plant expression vector and conjugated into Agrobacterium tumefaciens. The expression of the chimeric transgene was found to be induced by the pathogen Phytophthora infestans infection. The transgenic potato plants expressing 0.8 0.7 0.6 0.5

Hydrogen peroxide (μmol/g)

0.4 0.3 0.2 0.1 0 Wild-type plants Trangenic plants expressing fungal glucose oxidse

Fig. 3.26 Increased H2 O2 production in leaf tissues of transgenic potato plants expressing fungal glucose oxidase gene (Adapted from Wu et al. 1995)

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the fungal glucose oxidase gene under the control of the disease-inducible promoter showed enhanced resistance against the late blight pathogen P. infestans (Zhen et al. 2000). Transgenic rice plants overexpressing a fungal glucose oxidase gene showed enhanced accumulation of H2 O2 (Kachroo et al. 2003). These transgenic plants showed enhanced resistance to fungal and bacterial pathogens. However, constitutive expression of this gene caused improper seed set and decreased seed viability. It has been suggested that pathogen-inducible promoter may be useful to develop broad-spectrum disease resistant plants expressing the heterologous gene (Kachroo et al. 2003). The endogenous H2 O2 level was found to be enhanced in transgenic tobacco plants constitutively expressing the glucose oxidase gene isolated from Aspergillus niger. The transgenic tobacco plants showed enhanced resistance against the fungal pathogen Rhizoctonia solani and the bacterial pathogen Ralstonia solanacearum (Selvakumar et al. 2013). A glucose oxidase gene from A. niger was constitutively expressed under the CaMV 35S promoter in tobacco. The transgenic plants grew normally even though the glucose oxidase activity was higher in the transgenic tobacco plants. The transgenic tobacco plants showed resistance against the black shank pathogen Phytophthora nicotianae (Lee et al. 2002). Transgenic cabbage plants expressing the A. niger glucose oxidase gene showed resistance against the black rot bacterial pathogen Xanthomonas campestris pv. campestris. The disease resistance was positively associated with the glucose oxidase activity in leaves (Lee et al. 2002). However, the transgenic cabbage plants showed reduced seed set (Lee et al. 2002). Collectively these studies suggest that the fungal glucose oxidase is a potential tool to develop disease-resistant plants. However, accumulation of H2 O2 in plant tissues may affect the agronomic characters of the plants (Murray et al. 1999; Lee et al. 2002; Kachroo et al. 2003). This technology has to be fine tuned by using selective inducible promoters to express the gene at the appropriate time in the infection zone for effective disease management.

3.18 Manipulation of NO Signaling System to Activate Plant Immune Responses for Disease Management 3.18.1 Manipulation of S-Nitroso Glutathione Reductase (GSNOR) for Plant Disease Management Nitric oxide (NO) is a diffusible molecular messenger that plays an important role in plant immune responses (Vidhyasekaran 2014). S-nitrosothiols (SNOs) arising from the reaction of NO with sulfhydryl groups. S-nitrosothiols (SNOs) play important role in systemic acquired resistance (SAR). A reduction in NO accumulation leads to pathogen susceptibility (Delledonne et al. 1998; Zeidler et al. 2004) and by contrast, a decrease in SNO content promotes protection against microbial infection

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(Feechan et al. 2005). The important S-nitrosothiol in plants is S-nitrosoglutathione (GSNO) which is a NO reservoir and NO donor (Lindermayr et al. 2005). NO reacts rapidly with glutathione (GSH), the major intracellular low-molecular-mass antioxidant to yield S-nitrosoglutathione. GSNO is a bioactive, stable, and mobile reservoir of NO and it is an important player in plant defense responses against pathogens (Espunya et al. 2012). GSNO is considered to represent a functionally relevant signaling molecule that might act both as NO reservoir and NO donor (Lindermayr et al. 2005) or may act independently of homolytic cleavage to NO (Gaston 1999). GSNO acts synergistically with Salicylic acid (SA) in systemic acquired resistance (SAR) (Espunya et al. 2012). It has been suggested that GSNO would act as a long-distance phloematic signal in SAR (Durner and Klessig 1999). GSNO may be broken down by GSNO reductase (GSNOR) (Liu et al. 2001; Malik et al. 2011). A strong GSNO reductase activity has been demonstrated in plants (Lindermayr et al. 2005). NO system is regulated by GSNO reductase by inducing breakdown of GSNO (Liu et al. 2001). GSNOR reduces GSNO, an essential reservoir for NO activity (Wünsche et al. 2011). It is the main enzyme responsible for the in vivo control of intracellular levels of GSNO (Espunya et al. 2012). GSNOR controls not only the cellular levels of GSNO but also the levels of S-nitrosylated proteins (Grennan 2007). NO bioactivity is controlled by NO synthesis by the different routes and by NO degradation, which is mainly performed by the GSNOR (Liu et al. 2004). The loss of GSNOR function compromises defense responses in A. thaliana (Feechan et al. 2005). Mutation of the gene AtGSNOR1 in Arabidopsis controls cellular Snitrosothiols during plant-pathogen interactions (Feechan et al. 2005). GSNOR is encoded by a single-copy gene in Arabidopsis thaliana (Sakomoto et al. 2002). GSNOR has been shown to play a role in plant defense response (Rustérucci et al. 2007). SAR is impaired in plants overexpressing GSNOR and enhanced in the antisense plants, and this correlated with changes in the S-nitrosothiol (SNO) content both in local and systemic leaves. GSNOR was found to be localized in the phloem, suggesting that GSNOR would regulate SAR signal transport through the vascular system (Rustérucci et al. 2007). GSNOR controls SNO in vivo levels and the SNO content positively regulates plant defense responses (Feechan et al. 2005). GSNOR has been exploited to develop transgenic plants expressing resistance against oomycete and bacterial pathogens. Transgenic Arabidopsis plants with decreased amounts of GSNOR (S-nitroso glutathione reductase) (using antisense strategy) show enhanced basal resistance against Peronospora parasitica (Fig. 3.27; Rustérucci et al. 2007), which correlated with higher levels of S-nitrosothiols. Systemic acquired resistance induced by avirulent bacterial pathogen Pseudomonas syringae pv. phaseolicola is impaired in plants overexpressing GSNOR and enhanced in the antisense plants, and this correlates with changes in the S-nitrosothiol content both in local and systemic leaves (Rustérucci et al. 2007). The results suggest that NO signaling system can be manipulated by using antisense technology for plant disease management.

3.18 Manipulation of NO Signaling System to Activate …

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1000 900 800 700 600

Spores×104/g fresh wt

500 400 300 200 100 0 Wild-type plants AnƟsense GSNOR lines

Fig. 3.27 Transgenic Arabidopsis plants expressing antisense GSNOR show enhanced resistance against Peronospora parasitica (Adapted from Rustérucci et al. 2007)

3.18.2 Engineering Mammalian Nitric Oxide Synthase Gene for Crop Disease Management Nitric oxide synthase (NOS) is the key enzyme involved in NO production and NOS is a calmodulin (CaM)-binding protein (Vidhyasekaran 2016). NOS contains CaMbinding motifs and full activation of the enzyme needs both Ca2+ and CaM (Guo et al. 2003; Lamotte et al. 2004; Zeidler et al. 2004; Ma and Berkowitz 2007; Ma et al. 2008; Chun et al. 2012; Vidhyasekaran 2014). NO is synthesized predominantly by the enzyme NOS in mammals (Bethke et al. 2004). However, no obvious plant nitric oxide synthase homolog has yet been identified (Neill et al. 2008; Wilson et al. 2008). The PAMP-induced NO in tobacco cells has been shown to be reduced by NOS inhibitors, suggesting the occurrence of a NOS-like enzyme in plants (Lamotte et al. 2004). In Arabidopsis thaliana, a NOS-like enzyme, AtNOS1, has been identified and NO levels were found to be lower in the Atnos1 mutants impaired in AtNOS1 expression (Guo et al. 2003). NOS-like activity has been detected in various plants (Barroso et al. 1999; Wendehenne et al. 2001; Corpas et al. 2006). Inhibitors of mammalian NOS have been found to suppress NO production in plants (Zhang et al. 2003a, b; Lamotte et al. 2004; Zeidler et al. 2004; Mur et al. 2005, 2013; Zhao et al. 2007; Zottini et al. 2007). These observations suggest that NOS may be involved in NO generation in plants. However, a clear homologue of animal NOS has not yet been identified in plants (Guo et al. 2003; Crawford et al. 2006; Wilson et al. 2008). The plant enzyme displaying NOS-like activity is structurally different from classical mammalian NOS (Guo et al. 2003). Infiltration of mammalian NOS into plant cells triggers NO production and activation of plant immune responses (Durner et al. 1998). No genuine plant NOS gene has been cloned to date (Chun et al. 2012). Hence mammalian NOS isolated from rat brain has been used to develop transgenic plants expressing the mammalian NOS for inducing defense responses against various plant pathogens (Chun et al. 2012).

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The rat brain NOS (nNOS) cDNA, which was under the control of the constitutive Cauliflower Mosaic Virus (CaMV ) 35S promoter, was expressed in tobacco plants. These transgenic tobacco plants showed resistance against the bacterial pathogen Pseudomonas syringae pv. tabaci, the oomycete pathogen Phytophthora parasitica var. nicotianae and against the viral pathogen Tobacco mosaic virus (Chun et al. 2012). These results suggest that the mammalian NOS is a potential tool to develop transgenic plants expressing resistance against a wide range of pathogen. However these transgenic plants showed retarded shoot growth and probably use of inducible promoters may help to develop disease resistant plants without any adverse agronomic characters.

3.18.3 Manipulation of NO Signaling by Sodium Nitroprusside for Crop Disease Management Sodium nitroprusside (SNP) is a NO generator (Kobeasy et al. 2011; Thuong et al. 2015). SNP treatment triggered ROS and SA signaling systems. SNP treatment induced activities of peroxidase and phenylalanine ammonia-lyase in chilli (Capsicum annuum) (Thuong et al. 2015). Peroxidase is an important enzyme involved in ROS biosynthesis (Bolwell et al. 2002; Lehtonen et al. 2012; Vidhyasekaran 2014), whereas PAL is a key enzyme taking part in SA biosynthesis pathway (Lee et al. 1995; Vidhyasekaran 2015). Sodium prusside treatment effectively controlled chilli anthracnose disease caused by Colletotrichum capsici by eliciting defense responses (Thuong et al. 2015). Sodium nitroprusside applied as foliar spray effectively triggered host defense responses against Peanut mottle virus in peanut. This treatment enhanced the activities of various enzymes involved in ROS signaling system such as peroxidase, ascorbate peroxidase, catalase, and superoxide dismutase. Sodium nitroprusside treatment, besides inducing resistance against the PeMV virus in peanut, increased peanut seed protein and oil contents at harvest time. Also, the total unsaturated and saturated fatty acids content increased in the treated peanut seeds compared with the untreated ones (Kobeasy et al. 2011). These results suggest that sodium nitroprusside may be another potential tool to trigger plant immune system for effective crop management.

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Chapter 4

Bioengineering and Molecular Manipulation of Mitogen-Activated Kinases to Activate Plant Innate Immunity for Crop Disease Management

Abstract Plants have innate immune system to protect them against wide range of pathogens. However, the plant immune system is a sleeping system in unstressed healthy plants. Specific signaling systems have to be manipulated to trigger the expression of defense-related genes for effective management of crop diseases. The important components in the plant immune signal transduction system include calcium, reactive oxygen species, nitric oxide, salicylic acid, jasmonic acid, and ethylene—dependent signaling systems. The MAPKs transduce extracellular stimuli into intracellular transcription factors through activation of these signaling systems. A typical MAPK signaling module consists of three interconnected protein kinases: a MAP kinase kinase kinase (MAPKKK), a MAP kinase kinase (MAPKK), and a MAP kinase (MAPK). MAPKs act downstream of plant pattern recognition receptors (PRRs) and transduce extracellular stimuli into intracellular responses in plants. Although there are many MAPKs reported in plants, only a few of them are involved in plant immune signaling system and even among the few MAPKs, some regulate plant defense responses positively, while others regulate the defense responses negatively. The immunity-activating MAPKs also differ in activating the complex signaling systems. Technologies have been developed to utilize appropriate MAPK genes for developing disease-resistant plants. The MAPKs modulate phosphorylation of transcription factors to trigger transcription of defense genes. Bioengineering specific MAPK genes has been shown to induce disease resistance by triggering phosphorylation of transcription factors. BWMK1, the rice MAPK, phosphorylates the rice transcription factor OsEREBP1. EREBPs are known to bind to the GCC box DNA motif (AGCCGCC) that is located in the promoter of several PR genes. Transgenic tobacco plants expressing the rice BWMK1 gene show enhanced resistance against bacterial and oomycete pathogens. Some MAPK genes have been shown to regulate SA-mediated systemic acquired resistance (SAR). The cotton MAPK gene GhMPK7 and the maize MAPK gene ZmSIMK1 activate SA signaling system and transgenic plants overexpressing these genes show enhanced disease resistance.

© Springer Nature B.V. 2020 P. Vidhyasekaran, Plant Innate Immunity Signals and Signaling Systems, Signaling and Communication in Plants, https://doi.org/10.1007/978-94-024-1940-5_4

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Some MAPK genes (BnMPK4 and MK1) trigger the JA-mediated signaling system and these genes have been exploited to develop transgenic plants expressing enhanced resistance against necrotrophic pathogens. The cotton MAPK genes GhMPK16 and GHMPK2 activate SA, JA and ET signaling complex and these genes have been engineered to develop disease-resistant transgenic plants. Some mitogen-activated protein kinase kinase (MAPKK) genes have also been exploited to activate immune responses for crop disease management. The potato StMEK1DD gene was used for engineering for disease resistance. Transgenic potato plants carrying the StMEK1DD allele expressed from the pathogen-inducible potato vetispiradiene synthase (PVS) promoter showed resistance to various pathogens. Another MAPKK gene isolated from cotton, GhMKK5, has been utilised for developing disease-resistant Nicotiana benthamiana plants. The MAPKK gene MKK7 triggers accumulation of SA in Arabidopsis and the activation-tagged bud1 mutant, in which the expression of MKK7 is increased, shows enhanced resistance to pathogens. Some MAPK genes negatively regulate the defense responses and these genes also have been exploited to develop disease-resistant plants by knocking-out these MAPK genes. OsMPK6 knock-out plants showed SA-dependent systemic acquired resistance (SAR) against pathogens. MAPKs are negatively regulated by dephosphorylation through MAPK phosphatases (MKPs) Knockout of negative regulators of defense responses also could be a promising way for the production of disease-resistant plants. MKPs may nullify the function of the MAPKs in inducing resistance against necrotrophic pathogens. To overcome the negative function of the MKPs, MKP-suppressed plants have been developed. Tobacco plants in which NtMKP1 was silenced were produced by introducing an NtMKP1 antisense construct. These plants show enhanced resistance against the necrotrophic fungal pathogen. OsEDR1, a MAPKKK gene, negatively regulates disease resistance. Transgenic rice plants showing suppression of OsEDR1 expression were developed using RNAi strategy. The OsEDR1-RNAi plants show enhanced resistance against the rice bacterial blight pathogen. In another approach, OsEDR1knockout rice plants were developed. A rice mutant with T-DNA inserted in the fourth exon of OsEDR1 has been identified as OsEDR1-knockout plant. The transgenic OsEDR1-knockout plants show enhanced resistance against the bacterial pathogen. A kinase-deficient form of EDR1 gene has also been used to develop disease resistant plants. Overexpression of the kinase-deficient full-length EDR1 gene in wildtype Arabidopsis thaliana plants caused a dominant negative phenotype, conferring resistance to diseases. MAPK gene can also be manipulated to trigger the immune responses by using the biocontrol agent Trichoderma asperellum. A MAPK, designated as Trichoderma-induced MAPK (TIPK), has been identified and characterized in the Trichoderma-induced disease-resistant cucumber plants. The TIPK gene has been cloned and cucumber plants overexpressing the TIPK gene show resistance against pathogen. MAPK genes appear to be potential tools for developing disease resistant plants using various bioengineering technologies. Keywords MAPK signaling module · Phosphorylation of transcription factors · SA-mediated SAR · Transgenic plants · MAPKK genes · Allene oxide synthase · JA signaling system · Engineering MAPK genes · MAPKs in plant hormone

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signaling network · RNAi strategy · EDR1- knockout plants · Trichoderma-induced MAPK

4.1 MAPK Signal Transduction System in Plant Innate Immunity

Mitogen-activated protein kinases (MAPKs) are important components in the plant immune signal transduction system (Dóczi et al. 2007; Shen et al. 2010; Jammes et al. 2011; Liu et al. 2011; Shi et al. 2011; Vidhyasekaran 2014). They have pivotal roles in plant innate immunity (Pitzschke et al. 2009; Ishihama et al. 2011; Chujo et al. 2014). The MAPKs transduce extracellular stimuli into intracellular transcription factors through activation of calcium (Teige et al. 2004; Qi et al. 2010; Chujo et al. 2014), reactive oxygen species (Shi et al. 2011; Zhang et al. 2012b), nitric oxide (Kumar and Klessig 2000), salicylic acid (Zhang et al. 2007; Kobayashi et al. 2010; Shi et al. 2010), jasmonic acid (Gomi et al. 2005; Takahashi et al. 2007; Wang et al. 2009; Hiruma and Takano 2011; Kallenbach et al. 2010), and ethylene (Liu and Zhang 2004; Brader et al. 2007; Han et al. 2010; Shen et al. 2011; Zhang et al. 2011; Li et al. 2012)—dependent signaling systems, and enhance expression of defense-related genes in the plant innate immune system (Pedley and Martin 2004; Dóczi et al. 2007; Zhang et al. 2007; Beckers et al. 2009). A typical MAPK signaling module consists of three interconnected protein kinases: a MAP kinase kinase kinase (MAPKKK), a MAP kinase kinase (MAPKK), and a MAP kinase (MAPK) (Mészáros et al. 2006; Yang et al. 2015). MAP kinase cascade involves sequence of phosphorylation events (Hirt 2000; Ichimura et al. 2002; Li et al. 2012). MAPKs act downstream of plant pattern recognition receptors (PRRs) and transduce extracellular stimuli into intracellular responses in plants (Hettenhausen et al. 2012; Zhang et al. 2012a; Vidhyasekaran 2014). MAP kinase cascade components are abundant in plants (Cheong et al. 2003; Uppalapati et al. 2004; Nakagami et al. 2005; Hamel et al. 2006; Kandoth et al. 2007; Stulemeijer et al. 2007; Vidhyasekaran 2014; Yang et al. 2015). MAPKs constitute a large gene family with 20 family members in Arabidopsis, 15 in rice and 21 in Populus spp. (MAPK Group 2002; Hamel et al. 2006). More than 80 MAPKKKs, 10 MAPKKs and 20 MAPKs have been reported in Arabidopsis (Ichimura et al. 2002; Jonak et al. 2002; Nakagami et al. 2005). Although there are many MAPKs reported in plants, only a few of them are involved in plant immune signaling system. The MAPKK, NtMEK2, operates in the cascade upstream of SIPK and WIPK in tobacco cells. The constitutively active NtMEK2 induces the expression of defense genes (Yang et al. 2001; Zhang and Liu 2001). By contrast, other constitutively active tobacco MAPKKs neither activate SIPK or WIPK nor induce defense responses (Yang et al. 2001). MAPKs may regulate plant defense responses either positively or negatively. While some MAPKs positively regulate plant immune responses, there are MAPKs,

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which negatively regulate the immune responses. The Arabidopsis MAP kinases, MPK3 and MPK6, have been shown to be positive plant immune regulators (Takahashi et al. 2007; Ren et al. 2008; Beckers et al. 2009; Pitzschke et al. 2009; Liu et al. 2011). MPK3, MPK6, MKK4, and MKK5 form a cascade that positively regulates plant immune responses (Pitzschke et al. 2009). BnMPK4 positively regulates JA-mediated defense responses in oilseed rape (Wang et al. 2009). A cotton MAPK gene, GhMPK2, positively regulates plant defense responses (Zhang et al. 2011). Another cotton MAPK gene, GhMPK7, positively regulates the plant immune responses (Shi et al. 2010). A MAPKK encoding gene GhMKK5 from cotton has been isolated and characterized. The cotton MAPKK gene GhMKK5 also positively regulates plant defense responses. The expression of SA signaling system-inducible PR1a and PR5 and JA signaling system-inducible PR-4 genes was greatly elevated in GhMKK5-overexpressing plants (Zhang et al. 2012b). Another SA signaling pathway gene NPR1, which is involved in SAR response, was also significantly increased in GhMKK5-overexpressing plants (Zhang et al. 2012b). There are also MAPKs which negatively regulate the plant immune responses. In soybean, GmMPK4 is a negative regulator of SA, ROS, and defense responses. Silencing GmMPK4 resulted in activation of immune responses and it also led to elevated levels of SA and H2 O2 (Liu et al. 2011). MPK4, its upstream MAP kinase kinases MKK1 and MKK2, and the MAP kinase kinase kinase MEKK1 form a cascade that negatively regulates defenses in Arabidopsis (Gao et al. 2008; Qiu et al. 2008a; Pitzschke et al. 2009). EDR1 (ENHANCED DISEASE RESISTANCE 1) is a MAPKK Kinase (MAPKKK), which functions at the top of a MAP kinase cascade. The edr1 (enhanced disease resistance 1) gene encoding a putative MAPKKK negatively regulates SA signaling system (Frye et al. 2001).

4.2 Engineering Mitogen-Activated Protein Kinase (MAPK) Genes to Enhance Plant Immune Responses by Triggering Phosphorylation of Transcription Factors Transcription factors (TFs) are the master regulators of expression of genes involved in plant innate immune systems (Century et al. 2008; Jisha et al. 2015; Vidhyasekaran 2016). Transcription factors regulate the gene transcription processes by modulating the rate of transcription initiation of target genes (Du et al. 2009). The TFs are composed of four discrete domains, DNA binding domain, nuclear localization signal (NLS), transcription activation domain, and oligomerization site, which operate together to regulate the gene transcription processes by modulating the rate of transcription initiation of target genes (Du et al. 2009). TFs play important role in regulating defense gene expression and plant defense responses either positively (Century et al. 2008; Moreau et al. 2012) or negatively (Peng et al. 2010; Sun et al. 2010; Moreau et al. 2012).

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Induction of expression of genes encoding TFs appears to be critical in inducing disease resistance genes and conferring disease resistance (Cao et al. 2006; Waller et al. 2006; Zhang et al. 2007; van Verk et al. 2008). MAPK cascade has been shown to activate TFs involved in defense signaling system (Asai et al. 2002). The MAPKs modulate phosphorylation of transcription factors to trigger transcription of defense genes (Andreasson et al. 2005; Djamei et al. 2007; Liu et al. 2010; Ishihama et al. 2011; Mao et al. 2011). MPK3/MPK6 cascade has been shown to modulate the expression of the transcription factor WRKY33. MPK3/MPK6 phosphorylates WRKY33 in response to Botrytis cinerea infection in Arabidopsis. The phosphorylated WRKY33 transcription factor has been shown to induce the phytoalexin camalexin biosynthesis in Arabidopsis and induce disease resistance (Mao et al. 2011). The MAPKs, SIPK, WIPK, and NTF4 have been shown to phosphorylate WRKY8 transcription factor in Nicotiana benthamiana (Ishihama et al. 2011). Phosphorylation of WRKY8 increased its DNA binding activity to the cognate W-box sequence (Ishihama et al. 2011). The phosphorylated WRKY8 induces the expression of defense-related genes in N. benthamiana (Ishihama et al. 2011). The tobacco MAP kinase WIPK phosphorylates and activates NtWIF, a transcription factor, which triggers accumulation of transcripts for PR genes PR-1a and PR-2 (Waller et al. 2006). The bZIP transcription factor VIP1 is phosphorylated by MPK3 and the phosphorylated transcription factor regulates the expression of pathogenesis-related genes (Djamei et al. 2007; Liu et al. 2010). In rice, the OsMPK3/MPK6 activated by OsMKK4 phosphorylated OsWRKY53 recombinant protein at its multiple clustered serine-proline residues (SP cluster). When OsWRKY53 was coexpressed with a constitutively active mutant of OsMKK4, the enhanced transactivation activity of OsWRKY53 was found to be dependent on phosphorylation of the SP cluster (Chujo et al. 2014). An ERF transcription factor, ERF6, regulates defense gene expression in Arabidopsis. Phosphorylation of ERF6 by the MAPKs MPK3 and MPK6 increases ERF6 stability and the phosphorylated ERF6 activates the expression of defense-related genes (Meng et al. 2013). Technologies have been developed to utilize the MAPK genes for developing disease-resistant plants. Bioengineering specific MAPK genes has been shown to induce disease resistance by triggering phosphorylation of transcription factors. These MAPK genes can be exploited for crop disease management. BWMK1 (Blastand wounding-activated MAPK 1), a rice mitogen-activated protein kinase has been employed to develop disease-resistant transgenic plants (Cheong et al. 2003). BWMK1 is composed of an N-terminal kinase domain (KD) and an unusually long C-terminal extension domain (CD) that contains a putative Leu zipper motif (He et al. 1999). This protein phosphorylates the rice transcription factor OsEREBP1 (Oryza sativa ethylene-responsive element-binding protein 1). EREBPs are known to bind to the GCC box DNA motif (AGCCGCC) that is located in the promoter of several PR genes. In vitro phosphorylation of OsEREBP1 by BWMK1 enhanced its ability to bind to the GCC box DNA motif found in the promoters driving several PR genes. The cDNA of BWMK1 has been isolated from rice leaves challenged by the blast pathogen Magnaporthe oryzae (He et al. 1999). This gene encodes 506 amino acid

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protein that contains a dual-phosphorylation activation motif TDY (He et al. 1999). Ectopic expression of the BWMK1 in tobacco plant induced the expression of a broad spectrum of PR genes (Fig. 4.1; Cheong et al. 2003). The rice BWMK1 has been shown to be involved in the defense signaling system (Cheong et al. 2003). Transgenic tobacco plants were developed that constitutively express BWKM1 under the control of the Cauliflower mosaic virus (CaMV) 35S promoter. Overexpression of BWMK1 in transgenic tobacco plants induced hypersensitive-like cell death, accumulation of autofluorescent compounds such as phenolics, particularly lignin, and various PR proteins (Cheong et al. 2003). The transcript levels of PR-1, PR-2, PR-3, PR-4, and PR-5 genes were elevated in the transgenic plants. When the wild-type tobacco plants were inoculated with the oomycete pathogen Phytophthora parasitica var. nicotianae, the plants had severe disease symptoms, including leaf wilting and stem rot and most were dead 8 days BWMK1

Phosphorylation of OsEREBP1

Activation of OsEREBP1

Enhancement of DNA-binding ability of OsEREBP1 to bind to the GCC box motif in promoters of PR-1, PR-2, PR-3, PR-4, and PR-5 genes

Elevation of transcript levels of PR-1, PR-2, PR-3, PR4, PR-5 genes in transgenic tobacco plants expressing rice BWMK1 gene

Transgenic plants show enhanced disease resistance Fig. 4.1 BWMK1 phosphorylates OsEREBP1 transcription factor which binds to GCC box in the promoters of PR genes, driving expression of PR genes (Adapted from Cheong et al. 2003)

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Bacterial growth (log cfu/ml)

8 7 6 5 4 3 2 1 0 Wild-type plants

Transgenic plants expressing BWMK1 gene

Fig. 4.2 Transgenic tobacco plants expressing the BWMK1 gene show enhanced resistance against Pseudomonas syringae pv. tabaci (Adapted from Cheong et al. 2003)

after inoculation. By contrast, the transgenic plants overexpressing BWMK1 gene, remained healthy without any disease symptoms throughout the experimental period. The transgenic plants also showed enhanced resistance to the bacterial pathogen Pseudomonas syringae pv. tabaci. The in planta growth of the bacterium was about 100-fold less than in the wild-type plants (Fig. 4.2; Cheong et al. 2003). The results suggest that BWMK1 is a potential tool for developing disease-resistant plants.

4.3 Engineering Mitogen-Activated Kinase Kinase (MAPKK) Genes to Activate ROS Signaling System for Management of Crop Diseases Reactive oxygen species (ROS) signaling system plays a central role in launching the defense responses against a wide range of pathogens (L’Haridon et al. 2011; Lehtonen et al. 2012; Vidhyasekaran 2014). ROS mediates a reiterative signal network underlying systemic induced resistance (Lee and Hwang 2005). ROS appears to interact with various defense signaling systems. ROS induces NO signaling system (Bright et al. 2006), salicylic acid (SA) signaling system (Leon et al. 1995; Kauss and Jeblick 1995), ethylene (ET)-mediated signaling system (Vandenabeele et al. 2003), and jasmonic acid (JA)-dependent signaling system (Vranová et al. 2002; Vandenabeele et al. 2003). MAPK signaling cascades (MAPK kinase kinase [MAPKKK]-MAPKK-MAPK) have been shown to activate defense responses (Asai et al. 2002; Shen et al. 2010; Shi et al. 2011; Zhang et al. 2012c). NtMEK2, a

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% surviving plants without wil ng symptoms

tobacco MAPKK has been shown to activate both SA-induced protein kinase (SIPK) and wound-induced protein kinase (WIPK). Expression of NtMEK2DD , a constitutively active allele of NtMEK2, induced defense gene expression and generation of ROS (Yang et al. 2001; Ren et al. 2002; Yamamizo et al. 2006). The constitutively active mutant of potato ortholog of tobacco NtMEK2, StMEK1DD provokes SIPK and WIPK activities and induction of respiratory burst oxidase (NADPH oxidase) gene expression resulting in ROS production (Yoshioka et al. 2003). The potato StMEK1DD gene was used for engineering for disease resistance. Transgenic potato plants carrying the StMEK1DD allele expressed from the pathogen-inducible potato vetispiradiene synthase (PVS) promoter were developed (Yamamizo et al. 2006). The transgenic potato plants showed high accumulation of H2 O2 around the infection site. These plants showed resistance to Phytophthora infestans and Alternaria solani (Yamamizo et al. 2006). These studies suggest that by using the pathogen-inducible PVS promoter and a constitutive active allele of the master switch, StMEK1, we can enhance the defense response elicited during a compatible interaction to provide potato late blight resistance without the deleterious consequences of constitutive defense expression (Yamamizo et al. 2006). Another MAPKK gene isolated from cotton, GhMKK5, has been utilised for developing disease-resistant Nicotiana benthamiana plants (Zhang et al. 2012b). The overexpression of GhMKK5 in N. benthamiana showed enhanced resistance against the bacterial pathogen Ralstonia solanacearum. The wild-type plants inoculated with R. solanacearum showed severe wilting symptoms, while the transgenic plants overexpressing GhMKK5 were relatively less affected (Fig. 4.3; Zhang et al. 2012b). GhMKK5-overexpressing plants showed enhanced expression of NtRbohA gene encoding NADPH oxidase involved in accumulation of ROS. The transgenic plants 40 35 30 25 20 15 10 5 0 Wild-type plants Transgenic plants overexpressing GghMKK5

Fig. 4.3 Transgenic Nicotiana benthamiana pants overexpressing GhMKK5 gene from cotton show enhanced resistance to Ralstonia solanacearum (Adapted from Zhang et al. 2012b)

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also showed accumulation of H2 O2 , suggesting that GhMKK5 may be involved in ROS-mediated immune signaling system (Zhang et al. 2012b). These results reveal the potential of some MAPKK genes to develop disease-resistant plants.

4.4 Engineering MAPK/MAPKK Genes to Activate Salicylate Signaling System for Management of Diseases Salicylic acid (SA) signaling system plays a key role in activating plant innate immunity for effective disease management (Argueso et al. 2012; Fu et al. 2012; Denancé et al. 2013; Yang et al. 2013; Vidhyasekaran 2015). SA signaling system activates not only local resistance, but also systemic acquired resistance (SAR) observed in distal (systemic) tissues (Liu et al. 2011). The transgenerational SA-induced SAR has also been reported (Luna et al. 2012; Pieterse 2012). Some MAPK genes have been shown to regulate SA signaling system and induce disease resistance (Shi et al. 2010). GhMPK7 gene was isolated from cotton and transgenic Nicotiana benthamiana plants overexpressing GhMPK7 were developed. Transcript levels of SA pathway genes were more rapidly and strongly induced in the GhMPK7-overexpressing plants. These transgenic plants showed resistance to the fungal pathogen Colletotrichum nicotianae and also against the viral pathogen Potato virus Y (PVY). The transgenic plants germinated earlier and grew faster in comparison to wild-type plants (Shi et al. 2010). The results suggest that GhMPK7 is a potential tool to develop plants showing SA-regulated broad-spectrum disease resistance. A MAPK gene, ZmSIMK1, was isolated from maize (Zea mays) (Wang et al. 2014). Transgenic tobacco plants expressing the maize MAPK gene ZmSIMK1 were developed. Overexpression of ZmSIMK1 promoted the hypersensitive response (HR) and PR gene transcription. The transgene triggered SA-mediated systemic acquired resistance (SAR) against the bacterial pathogen Pseudomonas syringae pv. tomato in tobacco (Wang et al. 2014). It suggests that engineering ZmSIMK1 gene from maize is a useful technology for management of crop diseases. The MAPKK gene detected in Arabidopsis, MKK7, positively regulates plant basal and systemic acquired resistance. MKK7 has been shown to trigger accumulation of SA and the increases in SA levels resulted in enhanced expression of PR genes (Zhang et al. 2007). The activation-tagged bud1 mutant, in which the expression of MKK7 is increased, accumulates SA, exhibits constitutive PR gene expression, and displays enhanced resistance to both the oomycete pathogen Hyaloperonospora parasitica and the bacterial pathogen Pseudomonas syringae pv. maculicola (Zhang et al. 2007).

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4.5 Engineering MAPK Genes for Management of Pathogens by Activating JA Signaling System 4.5.1 MPK4 Genes JA signaling system has been shown to play important role in triggering defense responses against necrotrophic pathogens (Zheng et al. 2006; Wang et al. 2009; Zander et al. 2010; Méndez-Bravo et al. 2011; An and Mou 2013; Vidhyasekaran 2015). MAP kinase 4 (MPK4) acts as a positive regulator of JA signaling in plants (Petersen et al. 2000). Inactivation of MPK4 in mutant mpk4 Arabidopsis plants resulted in suppression of JA-responsive genes (Petersen et al. 2000). The MAPK module MEKK1-MKK1-MPK4 has been proposed to be responsible for JA biosynthesis in Arabidopsis thaliana (van Verk et al. 2011). A link between JA biosynthesis and the MAPK pathways has been reported in A. thaliana (van Verk et al. 2011). SA may suppress the biosynthesis of JA (Mur et al. 2006). SA has been suggested to suppress the expression of the JA biosynthetic enzymes lipoxygense (Spoel et al. 2003) and allene oxide synthase (Laudert and Weiler 1998). A large increase in JA levels has been reported in pathogen-challenged Arabidopsis NahG transgenic lines in which SA is suppressed (Spoel et al. 2003). The Arabidopsis mutants, which accumulate high levels of SA, show repression of JA-mediated pathway (Kachroo et al. 2003). SA strongly antagonized the JA signaling pathway, resulting in the downregulation of a large set of JA-responsive genes, including the marker genes PDF1.2 and VSP2 in Arabidopsis (Leon-Reyes et al. 2010). In the Arabidopsis aos/dde2 mutant, the expression of the JA biosynthesis enzyme allene oxide synthase (AOS) was completely blocked. Mutant aos/dde2 plants did not express the JA-responsive marker genes PDF1.2 or VSP2 in response to infection with the necrotrophic fungus Alternaria brassicicola. Bypassing JA biosynthesis by exogenous application of methyl jasmonate (MeJA) rescued this JA-responsive phenotype in aos/dde2. Application of SA suppressed MeJA-induced PDF1.2 expression to the same level in the aos/dde2 mutant as in wild-type plants (Leon-Reyes et al. 2010). The results suggest that SA may suppress JA-responsive gene expression. Activation of genes encoding key enzymes in the JA biosynthesis pathway, such as LOX29 (LIPOXYGENASE2), AOS (ALLENE OXIDE SYNTHASE), AOC2 (ALLENE OXIDE CYCLASE2), and OPR3 (12-OXO-PHYTODIENOATE REDUCTASE3) was repressed by SA (Fig. 4.4; Leon-Reyes et al. 2010). The MAP kinase MPK4 may suppress SA signaling system through which it may activate JA signaling system. MAP KINASE4 SUBSTRATE 1 (MKS1) is the target of MPK4 and phosphorylation of MKS1 by MPK4 has been reported to repress SA signaling. MKS1 interacts with the WRKY transcription factors WRKY25 and WRKY33 and both of them can be phosphorylated by MPK4 (Andreasson et al. 2005). Overexpression of both WRKY25 and WRKY33 results in repression of SA signaling responses, suggesting that these transcription factors, after activation by phosphorylation by the action of MPK4, suppress SA signaling system (Zheng et al. 2006, 2007). By contrast, wrky33 mutant plants showed reduced expression

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ɲ- Linolenic acid

SA

LOX2 gene expression

Lipoxygenase

13S-hydroperoxyoctadecatrienoic acid

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AOS1 gene expression

Allene oxide synthase

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AOC2 gene expression

Allene oxide cyclase

12-oxo-phytodienoic acid (OPDA)

SA

OPR3 gene expression

OPDA reductase OPC 8:0

inhibiƟon SA

JA biosynthesis

Fig. 4.4 Inhibition of JA biosynthesis by SA (Adapted from Leon Reyes et al. 2010)

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of JA-responsive genes, suggesting that WRKY33 after phosphorylation by MPK4 activates JA signaling system (Zheng et al. 2006). These studies suggest that MPK4 activates JA signaling system by suppressing SA signaling system. Hence the MPK4 gene can be engineered to overexpress JA signaling system for management of diseases caused by necrotrophic pathogens. MPK4 gene has been detected in Arabidopsis (Petersen et al. 2000; Brodersen et al. 2006; Brader et al. 2007; Gao et al. 2008; Hettenhausen et al. 2012), Nicotiana tabacum (Gomi et al. 2005), N. attenuata (Wu et al. 2007), Brassica napus (Wang et al. 2009), soybean (Liu et al. 2011), and rice (Shen et al. 2010). BnMPK4 gene was cloned from oilseed rape (Brassica napus) and transgenic B. napus plants overexpressing the BnMPK4 gene were developed (Wang et al. 2009). The transgenic plants showed enhanced resistance against the necrotrophic fungal pathogen Sclerotinia sclerotiorum. Enhanced resistance in the transgenic lines was due to both delay of lesion occurrence and slow lesion expansion rate (Wang et al. 2009). The transgenic plants also showed enhanced resistance against another necrotrophic fungal pathogen Botrytis cinerea (Fig. 4.5; Wang et al. 2009). High levels of BnMPK4 transcription in the transgenic plants were shown to activate expression of the defensin gene PDF1.2 but suppress the PR-1 gene expression. PDF1.2 gene is considered as a marker gene for the JA-mediated defense pathway, whereas PR-1 is considered as a marker gene for SA mediated signaling pathway. These results suggest that BnMPK4 gene can be employed to develop disease-resistant plants for management of necrotrophic pathogens by activating JA signaling system. 100 90 80 70 60

% spreding lesions 50 40 30 20 10 0 Wild-type plants Transgenic plants

Fig. 4.5 Transgenic Brassica napus plants overexpressing BnMPK4 gene show enhanced resistance to Botrytis cinerea (Adapted from Wang et al. 2009)

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4.5.2 MK1 Gene from Capsicum Annuum A MAPK gene, MK1 (Mitogen-activated protein kinase 1) has been cloned from Capsicum annuum. It is transcriptionally, translationally, and posttranslationally induced in wounded C. annuum plants (Shin et al. 2001). MK1 is highly conserved in plants and it shares 92% amino acid identity with wound-induced protein kinase (WIPK) from tobacco (Lee et al. 2004). The MK1 gene from C. annuum was introduced into the rice genome by Agrobacterium-mediated transformation (Lee et al. 2004). The constitutive expression of the MK1 transgene in rice plants was found to increase the basal level of jasmonic acid. The transgenic rice plants expressing MK1 gene from C. annuum showed resistance against the blast pathogen Magnaporthe oryzae (Lee et al. 2004). The results suggest that the MAPK gene MK1 may be a potential tool to develop transgenic plants expressing disease resistance.

4.6 Engineering MAPK Genes to Activate Salicylate-Jasmonate-Ethylene Signaling Network for Crop Disease Management 4.6.1 MAPKs Activate Plant Hormone Signaling Network Various plant hormone signaling systems differentially regulate plant defense responses against biotrophic, hemibiotrophic, necrotrophic, fungal, oomycete, bacterial, and viral pathogens in crop plants (Hénanff et al. 2013; Xu et al. 2013; Vidhyasekaran 2015). It has been demonstrated that specific signaling pathways should be activated to confer resistance against specific pathogens. SA-mediated signaling plays a key role in triggering defense responses against biotrophic and hemibiotrophic fungal and oomycete pathogens (Thomma et al. 2001a, b; Fan et al. 2009; Slaughter et al. 2012). SA induces resistance against hemibiotrophic bacterial pathogens (Naseem et al. 2012; Son et al. 2012). It also triggers resistance against several viral pathogens (Kachroo et al. 2000; Love et al. 2005; Sänchez et al. 2010). JA-mediated pathway effectively confers resistance against necrotrophic pathogens (Berrocal-Lobo and Molina 2004; McGrath et al. 2005; Zheng et al. 2006; MéndezBravo et al. 2011; El Rahman et al. 2012; Wild et al. 2012; Vidhyasekaran 2015). ET signaling confers resistance against Erwinia carotovora in Arabidopsis (Thomma et al. 2001a). ET signaling system induced resistance against the necrotrophic fungal pathogens Botrytis cinerea and Cercospora nicotianae and the necrotrophic bacterium Erwinia carotovora. By contrast, the ET system did not induce resistance against the biotrophic fungus Oidium neolycopersici and induced susceptibility against the oomycete Peronospora tabacina and Tobacco mosaic virus in tobacco (Geraats et al. 2003).

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In some cases, both JA and SA signaling systems are required to confer resistance against pathogens. Both JA and SA are required to confer resistance to Pseudomonas syringae and Hyaloperonospora parasitica in Arabidopsis (Clarke et al. 2000; Nandi et al. 2003). Plectosphaerella cucumerina is controlled by SA-dependent as well as by JA-dependent defense responses in A. thaliana (Thomma et al. 2001a). JA, ET, and SA play significant roles in disease resistance against Pythium irregulare (Adie et al. 2007). These studies suggest that activation of multiple hormone signaling pathways may be needed to induce resistance against a wide range of pathogens (Hénanff et al. 2013). MAPK signaling cascade has been shown to activate SA, JA, and ET signaling systems. The MAPKK gene MKK7 positively regulates plant basal and systemic acquired resistance. MKK7 has been shown to trigger accumulation of SA and the increases in SA levels resulted in enhanced expression of PR genes (Zhang et al. 2007). MAPKs have been shown to trigger JA signaling system (Lee et al. 2004; Teige et al. 2004; Seo et al. 2007; Kobayashi et al. 2010). The mitogen-activated protein kinase WIPK-overproducing tobacco plants showed 3- to 4-fold higher levels of JA than in the wild type plants (Seo et al. 1999). The MKK2 overexpressor lines showed increased expression of lipoxygenase gene involved in JA biosynthesis (Teige et al. 2004). MAPKs are also involved in activation of ET signaling system. MPK3/6, together with their upstream MKK9 or MKK4/5, functions in the ethylene biosynthesis pathway (Liu and Zhang 2004; Menke et al. 2004; Joo et al. 2008; Xu et al. 2008). In tobacco, activation of the MAP kinase cascade has been reported to cause an increase in ethylene levels (Kim et al. 2003a; Ren et al. 2006). MAP kinases phosphorylate the ethylene biosynthetic enzymes ACC synthases 2 and 6, (ACS2 and 6) leading to their stabilization (Liu and Zhang 2004; Yoo et al. 2008). The MAP kinase MPK6 phosphorylates ACS2/6, resulting in increased ethylene production (Boutrot et al. 2010). SA and JA/ET signaling systems may induce distinctly different PR proteins (Vidhyasekaran 2015). Some PR proteins are induced by JA. PR4 is induced by JA in rice (Agrawal et al. 2003) and maize (Bravo et al. 2003). JA induced the thaumatin-like protein of the PR-5 family in Pinus monticola, while SA did not induce it (Piggott et al. 2004). PR1 is known as a marker gene for the SA signaling pathway, and PR4 and PDF1.2 are markers for the JA/ET pathway (Shi et al. 2011). Plants overexpressing MAPK genes show enhanced expression of various PR genes, which are activated by SA, JA, and ET signaling systems (Shi et al. 2011). These studies suggest that MAPK genes may be potential tools for engineering for disease resistance by activating SA, JA, and ET signaling systems.

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4.6.2 Cotton GhMPK16 Gene A cotton MAPK gene, GhMPK16, was employed to develop disease-resistant plants by activating SA, JA and ET signaling systems (Shi et al. 2011). GhMPK16 is a group D MAP kinase identified in cotton. GhMPK16 has an activation loop (Tloop), a phosphorylation motif (TDY motif) in the T loop and an extended C-terminal region. It lacks a C-terminal CD domain. The protein is localized in the nucleus. The cotton pathogens Xanthomonas campestris pv. malvacearum, Colletotrichum gossypii and Fusarium oxysporum f. sp. vasinfectum elevated the transcription level of GhMPK16 in cotton during the infection process (Shi et al. 2011). The usefulness of the GhMPK16 gene to develop disease-resistant plants was assessed by transforming the coding sequence of the gene into Arabidopsis plants. The GhMPK16 overexpressing Arabidopsis plants showed enhanced resistance against the bacterial pathogen Ralstonia solanacearum. The transgenic plants also showed enhanced resistance against the fungal pathogens Cercospora nicotianae and Alternaria alternata (Fig. 4.5; Shi et al. 2011). The transgenic plants showed increased expression of SA, JA, and signaling pathways-mediated PR genes, when challenge-inoculated with R. solanacearum. PR1 is a marker gene for the SA signaling system while PDF1.2 is a marker gene for the JA signaling pathway, and PR4 is the marker gene for ET signaling pathway. All the three marker genes were strongly induced in the transgenic plants than in the wild-type plants (Shi et al. 2011). The results suggest that the GhMPK16 can be engineered to develop plants with enhanced resistance against a wide spectrum of pathogens by activating all three hormone signaling pathways.

4.6.3 Cotton GhMPK2 Gene A MAPK gene, GhMPK2, isolated from cotton is a potential gene which can be exploited to develop disease-resistant plants (Zhang et al. 2011). The GhMPK2 cDNA isolated from cotton was inserted into the binary vector pBI121 under the control of the cauliflower mosaic virus 35S promoter. Tobacco plants were transformed with the gene construct. The transgenic tobacco plants constitutively expressing GhMPK2 showed enhanced resistance against various viral, oomycete and fungal diseases. These plants showed resistance against Cucumber mosaic virus (CMV) and Tobacco mosaic virus (TMV). The virus accumulation in the transgenic plants was much lower than in the wild-type plants (Fig. 4.6; Zhang et al. 2011). Severe disease symptoms were observed within 14 days after inoculation with CMV or TMV in the wild-type plants. However, only slight disease symptoms were observed in the transgenic plants. The transgenic tobacco plants overexpressing the cotton GhMPK2 gene showed enhanced resistance against the oomycete black shank pathogen Phytophthora parasitica. The wild-type plants exhibited typical black shank disease symptoms at 10 days postinoculation with the pathogen, while the transgenic plants showed less

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Virus 1.2 accumula on (absorbance at 1 490 nm)

Wild-type plants Transgenic plants

0.8 0.6 0.4 0.2 0 TMV

CMV

Fig. 4.6 Transgenic tobacco plants overexpressing GhMPK2 show enhanced resistance against Tobacco mosaic virus (TMV) and Cucumber mosaic virus (CMV) (Adapted from Zhang et al. 2011)

severe or no disease symptoms (Zhang et al. 2011). The transgenic tobacco plants also showed resistance against the fungal wilt pathogen Fusarium oxysporum (Zhang et al. 2011). These results suggest that the GhMPK2 gene can be engineered to develop plants expressing resistance against wide spectrum of pathogens. The transgene appears to trigger expression of genes involved in ethylene, SA, and JA signaling pathways activating defense responses. The transcriptional levels of ACS encoding 1-amino cyclopropane-1-carboxylic acid (ACC) synthase and ACO gene encoding ACC oxidase were significantly increased in the transgenic plants without any treatment (Fig. 4.7; Zhang et al. 2011). Both these enzymes are involved in ET biosynthesis. These results suggest that GhMPK2 triggers the ET biosynthesis pathway. The transgenic plants overexpressing GhMPK2 showed enhanced expression of PR1a, PR2, PR4, and PR5 genes. Transcripts of these genes were significantly upregulated in the transgenic plants (Zhang et al. 2011). The PR genes encoding pathogenesis-related (PR) proteins play important role in conferring disease resistance (Vidhyasekaran 2007). PR-1a and PR5 are the marker genes for SA signaling and PR4 is the marker gene for JA signaling (Vidhyasekaran 2015). These results suggest that GhMPK2 may activate ET, JA, and SA signaling systems to trigger immune responses for disease management.

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S-adenosyl-L-methionine (S-Ado-Met)

GhMPK2

Increases in ACS gene transcription

ACC synthase (ACS)

ACC

GhMPK

Increases in ACO gene transcription

ACC oxidase (ACC)

Ethylene

Fig. 4.7 GhMPK2 triggers activation of genes involved in ethylene biosynthesis pathway (Adapted from Zhang et al. 2011)

4.7 Molecular Manipulation of MAPK Genes Which Negatively Regulate SA Signaling System for Crop Disease Management 4.7.1 Manipulation of Arabidopsis MPK4 Gene MPK4, its upstream MAP kinase kinases MKK1 and MKK2, and the MAP kinase kinase kinase MEKK1 form a cascade that negatively regulates SA signaling system in Arabidopsis (Petersen et al. 2000; Mészáros et al. 2006; Qiu et al. 2008a; Pitzschke et al. 2009). The mpk4 plants exhibit constitutive systemic acquired resistance, including elevated salicylic acid levels and increased resistance to virulent pathogens (Petersen et al. 2000). The mekk1/mkk1/mkk2 double mutants also display similar elevated levels of SA (Petersen et al. 2000; Gao et al. 2008; Qiu et al. 2008b). The results suggest that the three kinase module involving MEKK1-MKK1/2-MPK4 negatively regulates SA biosynthesis and signaling system. To exploit the negatively regulating MPK4 gene for developing disease-resistant plants, mpk4 mutant plants were developed. The mpk4 mutant was identified among stable transposant lines generated with a modified maize Ds element (Sumdaresan et al. 1995). The Ds was found to be integrated eight nucleotides upstream of the acceptor site of the first intron of MPK4. This insertion was responsible for the mpk4 phenotype (Petersen et al. 2000). The PR genes PR1, PR2, and PR5, which are

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Fig. 4.8 Accumulation of salicylic acid in Arabidopsis mpk4 mutant plants (Adapted from Petersen et al. 2000)

normally induced during the development of systemic acquired resistance (SAR), were constitutively expressed in mpk4 plants (Petersen et al. 2000). SA content was higher in mpk4 plants (Fig. 4.8; Petersen et al. 2000). PR1 gene expression in mpk4 was found to be fully-dependent upon SA. SA and SA glucosides (SAG) levels were 9- and 25-fold higher in mpk4 plants (Petersen et al. 2000). The results suggest that MPK4 functions upstream of SA in SAR signaling. The mpk4 plants were found to be highly resistant to the bacterial pathogen Pseudomonas syringae pv. tomato Dc3000. The mpk4 plants also showed resistance to the oomycete pathogen Hyaloperonospora parasitica. The oomycete pathogen rapidly colonized and caused disease symptoms on wild-type plants but was undetectable in mpk4 plants (Petersen et al. 2000). The results suggest that the MAPK gene MPK4 can be manipulated to develop disease-resistant plants.

4.7.2 Manipulation of GmMPK4 Soybean (Glycine max) plants were silenced for various MAPKs, MAPKKs, and MAPKKKs using virus-induced gene silencing mediated by Bean pod mottle virus (Liu et al. 2011). Among the soybean plants silenced for various MAPKs, MAPKKs, and MAPKKKs, those in which GmMPK4 homologs were silenced, showed increased resistance to downy mildew and Soybean mosaic virus. SA accumulation was significantly increased in GmMPK4-silenced plants (Liu et al. 2011). GmMPK4 negatively regulates SA signaling pathway and silencing of the MAPK gene activates the SA-dependent pathway inducing disease resistance (Liu et al. 2011). The results suggest that GmMPK4 gene is another potential tool for management of oomycete and virus diseases.

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18 16 14 12

Salicylic acid (μg/g fresh wt)

10 8 6 4 2 0 Wild-type plant

OsMPK6knockout plant

Fig. 4.9 Increases in SA biosynthesis in OsMPK6-knockout plants (Adapted from Shen et al. 2007)

4.7.3 Manipulation of OsMPK6 Gene The rice mitogen-activated protein kinase OsMPK6 has been shown to play important role in regulating rice disease resistance (Yuan et al. 2007; Shen et al. 2010). It negatively regulates rice disease resistance against bacterial pathogens (Yuan et al. 2007). Suppressing OsMPK6 in rice plants results in enhanced resistance to different races of the bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Shen et al. 2010). The OsMPK6 knock out mutant rice plants showed enhanced resistance against the bacterial blight pathogen (Shen et al. 2010). OsMPK6 knock-out plants showed higher accumulation of SA (Fig. 4.9; Shen et al. 2010). OsMPK6 knockout plants also showed SA-dependent systemic acquired resistance (SAR) against the bacterial pathogen. PR1a expression was markedly induced in both infected and systemic healthy leaves in OsMPK6 knock-out plants (Shen et al. 2010). These results suggest that disease-resistant plants can be developed by knocking out the OsMPK6 gene and these plants may also show SAR.

4.8 Molecular Manipulation of SIPK-WIPK Genes Expression for Crop Disease Management Two mitogen-activated protein kinases, salicylic acid-induced protein kinase (SIPK) and wound-induced protein kinase (WIPK) are involved in conferring resistance against necrotrophic pathogens by activating JA/ET signaling system (Oka et al. 2013). WIPK and SIPK function cooperatively to regulate JA or ET biosynthesis (Seo et al. 2007; Kobayashi et al. 2010). MAPKs are negatively regulated by dephosphorylation through MAPK phosphatases (MKPs) (Kerk et al. 2002; Schweighofer et al. 2007). The tobacco MKP NtMKP1 inactivates salicylic acid-induced protein

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kinase (SIPK) through dephosphorylation of the TEY motif of SIPK (Katou et al. 2005). The phosphatase activity of NtMKP1 was increased strongly by the binding of SIPK and weakly by another MAPK, WIPK (Katou et al. 2005). NtMKP1 dephosphorylates and inactivates SIPK in vitro (Katou et al. 2005). In transgenic tobacco plants overexpressing NtMKP1, the activation of both WIPK and SIPK was suppressed and JA production after wounding was also suppressed (Seo et al. 2007). JA signaling system confers resistance against necrotrophic pathogens (Thatcher et al. 2009; Moffat et al. 2012; Vidhyasekaran 2015). WIPK/SIPKs are involved in triggering resistance against necrotrophic pathogens. However. MKPs may inactivate the MAPKs and suppress the JA signaling system. MKPs may nullify the function of the MAPKs in inducing resistance against necrotrophic pathogens. To overcome the negative function of the MKPs, MKP-suppressed plants have been developed (Oka et al. 2013). Tobacco plants in which NtMKP1 was silenced were produced by introducing an NtMKP1 antisense construct under the control of an enhanced 35S promoter (Oka et al. 2013). NtMKP1-suppressed tobacco lines exhibited enhanced production of JA and ET. These plants showed enhanced resistance against the necrotrophic fungal pathogen Botrytis cinerea (Fig. 4.10; Oka et al. 2013). The results suggest that knockout of negative regulators of defense responses could be a promising way for the production of disease-resistant plants.

30 25 20

Lesion size (mm) 15 10 5 0 Control

NtMKP1suppressed transgenic lines

Fig. 4.10 NtMKP1-suppressed tobacco plants show enhanced resistance against Botrytis cinerea (Adapted from Oka et al. 2013)

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4.9 Molecular Manipulation of EDR1, a MAPKK Kinase for Plant Disease Management The gene EDR1 (ENHANCED DISEASE RESISTANCE 1) encodes a MAPK Kinase Kinase (MAPKKK), which functions at the top of a MAP kinase cascade. EDR1 gene has been isolated from Arabidopsis and putative orthologs of EDR1 have been detected in maize, rice and tomato (Frye et al. 2001). EDR1 has been shown to negatively regulate disease resistance (Frye and Innes 1998; Frye et al. 2001; Shen et al. 2010). The edr1 mutant exhibits enhanced resistance against the powdery mildew pathogen Golovinomyces cichoracearum in Arabidopsis thaliana (Frye and Innes 1998; Frye et al. 2001), suggesting that EDR1 acts as a negative regulator of defense responses. Suppression of OsEDR1 in rice enhanced resistance to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae, suggesting that OsEDR1, the ortholog of Arabidopsis EDR1 negatively regulates disease resistance (Shen et al. 2010). EDR1 negatively regulates SA signaling system. All EDR1-associated phenotypes are suppressed by mutations that block SA perception (nim1) or reduce SA production (pad4 and eds1). The NahG transgene, which lowers endogenous SA levels, also suppressed EDR1 expression (Frye et al. 2001). These results suggest that EDR1 plays an important role in SA-mediated defense responses. Plant defensin PDF genes are downregulated in edr1 mutants. PDF1.2 (PR-12; defensin), is an important pathogenesis-related protein involved in plant innate immune responses (Vidhyasekaran 2007) and its expression is triggered by the JA signaling system (Jung et al. 2007; Oñate-Sánchez et al. 2007; Pré et al. 2008). MYC2/JIN1 encodes a basic helix-loop-helix leucine zipper transcription factor and differentially regulates JA-responsive defense genes (Lorenzo et al. 2004). MYC2 is involved in repression of PDF1.2 expression and PDF1.2 was highly induced in edr1myc2 double mutant (Hiruma and Takano 2011). It has been shown that EDR1 is critical for expression of plant defensin genes and the MYC2-encoded transcription factor represses defensin expression. Inactivation of MYC2 fully restored defensin expression in edr1 mutants (Hiruma and Takano 2011). It suggests that EDR1 cancels MYC2 function to regulate defensin expression. The edr1 mutant of Arabidopsis confers resistance against bacterial and fungal pathogens. When the edr1 plants were inoculated with the powdery mildew pathogen Golovinomyces cichoracearum, the mutant plants showed increased expression of several defense-related genes (Christiansen et al. 2011). Many of the genes with elevated expression encoded WRKY transcription factors. EDR1 was found to be localized to the nucleus, suggesting that EDR1 could potentially interact with transcription factors in the nucleus (Christiansen et al. 2011). OsEDR1 is a sequence ortholog of Arabidopsis EDR1. It has been shown that OsEDR1 negatively regulates plant defense responses via the activation of ethylene biosynthesis (Shen et al. 2011). OsEDR1-suppressing knockout (KO) rice plants showed enhanced resistance against the bacterial blight pathogen Xanthomonas oryzae pv. oryzae. This resistance was associated with increased accumulation of SA

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and JA, induced expression of SA- and JA-related defense genes and suppressed accumulation of 1-aminocyclopropane-carboxylic acid (ACC), the precursor of ethylene, and expression of ethylene-related genes. Knockout of OsEDR1 suppressed the ACC synthase (ACS) gene family, which encodes the enzymes of ethylene biosynthesis by catalyzing the formation of ACC. The enhanced disease resistance of the OsEDR1knockout plants was complemented by ACC treatment. ACC treatment decreased SA and JA biosynthesis in OsEDR1-knockout plants. In contrast, aminoethoxyvinylglycine, the inhibitor of ethylene biosynthesis promoted expression of SA and JA synthesis-related genes in OsEDR1-knockout plants (Shen et al. 2011). These studies show that OsEDR1 transcriptionally promotes the synthesis of ethylene that, in turn, suppresses SA- and JA-associated defense signaling. The OsEDR1-knockout plants may be associated with activation of SA- and JA-associated defense transduction pathways and suppression of the ethylene-associated pathway. OsEDR1 gene has been exploited to develop disease resistant rice plants. Shen et al. (2010) developed transgenic plants showing suppression of OsEDR1 expression using RNAi strategy. The OsEDR1-RNAi plants showed enhanced resistance against the rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae. All the resistant transgenic plants showed reduced OsEDR1 transcripts compared with wildtype plants. In another approach, OsEDR1-knockout rice plants were developed. The OsEDR1 gene consisted of 13 exons and 12 introns. A rice mutant with T-DNA inserted in the fourth exon of OsEDR1was identified as OsEDR1-knockout plant (Shen et al. 2010). All the transgenic OsEDR1-knockout plants showed enhanced resistance against the bacterial pathogen (Fig. 4.11; Shen et al. 2010). The enhanced resistance was associated with suppressed expression of OsEDR1 (Shen et al. 2010). A kinase-deficient form of EDR1 gene has also been used to develop disease resistant plants. Full-length EDR1 cDNA was cloned into the pGEMT vector. To produce a kinase-deficient EDR1 construct, a conserved lysine residue at position 696 was substituted with a methionine using a two-step recombinational PCR method 70 60 50 40

Disease area (%) 30 20 10 0 Wild-type plants

OsEDR1 - knock out plants

Fig. 4.11 OsEDR1-knock-out rice plants show enhanced resistance against the bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Adapted from Shen et al. 2010)

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(Tang and Innes 2002). The wild-type and kinase-deficient mutant EDR1 cDNAs were then excised from pGEMT and inserted into the pBI1.41vector, which contains a modified 35S CaMV promoter (Tang and Innes 2002). Overexpression of the kinase-deficient full-length EDR1 gene (35S::dnEDR1) in wild-type Arabidopsis thaliana plants caused a dominant negative phenotype, conferring resistance to powdery mildew pathogen Erysiphe cichoracearum. The 35S::dnEDR1 transgene was found to be highly transcribed in transgenic plants (Tang and Innes 2002). It has been suggested that overexpression of orthologous dnEDR1 constructs may provide a novel strategy for controlling powdery mildew disease in crop plants (Tang and Innes 2002).

4.10 Manipulation of TIPK Gene Using Trichoderma for Crop Disease Management Trichoderma asperellum (Trichodema harzianum 203) is an effective biocontrol agent which has been exploited for the management of various crop diseases (Segarra et al. 2010, 2012; Wijesinghe et al. 2011; Mbarga et al. 2012; de Franca et al. 2015; El Komy et al. 2015). T. asperellum can penetrate the roots of cucumber (Cucumis sativus) seedlings and colonize the epidermis and outer cortex (Yedidia et al. 1999). Preinoculation of roots with T. asperellum activates plant defense mechanisms. A MAPK, designated as Trichoderma-induced MAPK (TIPK), was identified and characterized in the induced disease-resistant cucumber plants (Shoresh et al. 2006). The TIPK mRNA levels increased in the Trichoderma-inoculated roots, peaking 4- to 5-fold in untreated plants. The expression levels of the TIPK gene also increased in the leaves after treatment of roots (Fig. 4.12; Shoresh et al. 2006). Expression of the 60 50 40

Rela ve TIPK 30 mRNA levels 20 10 0 Mock-inoculated plants

Trichodermainoculated plants

Fig. 4.12 Induction of TIPK gene expression in cucumber leaves after Trichoderma inoculation on the cucumber roots (Adapted from Shoresh et al. 2006)

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TIPK gene in leaves suggests a systemic gene response to root inoculation of Trichoderma in cucumber (Shoresh et al. 2006). Inoculation of T. asperellum on roots of cucumber plants induced systemic resistance against leaf infection by the bacterial pathogen Pseudomonas syringae pv. lachrymans (Shoresh et al. 2005). The results suggest that T. asperellum is a potential tool to trigger induced systemic resistance in cucumber. The TIPK gene was cloned and cucumber plants overexpressing the TIPK gene were developed. Plants overexpressing TIPK were more resistant to P. syringae pv. lachrymans than control plants (Shoresh et al. 2006). On the other hand, plants expressing TIPK—antisense RNA showed increased sensitivity to pathogen attack. Moreover, Trichoderma pre-inoculation could not protect the antisense cucumber plants (Shoresh et al. 2006). The results suggest that Trichoderma exerts its protective effect on plants through activation of the TIPK gene.

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Chapter 5

Bioengineering and Molecular Manipulation of Salicylic Acid Signaling System to Activate Plant Immune Responses for Crop Disease Management

Abstract Plant innate immune system provides potential weapons to the plants for fighting against pathogens. However, specific signals are needed to activate the system. Salicylic acid (SA) is the most important endogenous signal molecule which triggers the plant defense system. Plants do not have much endogenous SA. Increased synthesis and accumulation of salicylic acid in plants result in increased expression of defense genes. It has been shown that by increasing the SA content, defense genes can be activated and diseases can be controlled. Several molecular technologies have been developed to increase the biosynthesis of SA by engineering genes encoding enzymes involved in SA biosynthesis. Isochorismate synthase (ICS) and isochorismate pyruvate lyase (IPL) are the key enzymes involved in biosynthesis of SA. The genes encoding ICS and IPL cloned from two different bacteria have been exploited to develop disease-resistant plants by triggering SA accumulation. Transgenic tobacco plants expressing both the ICS and IPL genes show high increase in SA accumulation and these plants show enhanced disease resistance against Tobacco mosaic virus and the powdery mildew pathogen Oidium lycopersici. The regulatory protein PAD4 is known to activate SID1 and SID2. SID2 is an isochorismate synthase that is involved in SA biosynthesis and SID1 encodes a protein, which transports precursors for SA biosynthesis. Transgenic wheat plants overexpressing the Arabidopsis PAD4 coding sequence have been developed and these transgenic plants show accumulation of SA and resistance against the Fusarium head blight (FHB) pathogen Fusarium graminearum. A RNA-binding protein (RBP) gene from Arabidopsis thaliana, AtRBP-DR1 has been exploited for developing disease-resistant plants by inducing SA biosynthesis. A camodulin binding protein, CBP60g, has been exploited to develop disease resistant plants by activating SA biosynthesis. Transgenic Arabidopsis plants overexpressing CBP60g gene have been developed and these plants show elevated SA accumulation and enhanced resistance against diseases. Several transcription factors are known to take part in the regulation of SA signaling pathway and genes encoding these transcription factors have been exploited to develop disease-resistant plants. Ubiquitin- and proteasome-mediated degradation of proteins plays an important role in plant defense signaling system. E3 ubiquitin ligases play a key role in the ubiquitin-proteasome system. Ubiquitin-proteasome pathway has been manipulated to trigger SA signaling system for crop disease management. NPR1 gene is a master regulator of the SA-mediated induction of systemic © Springer Nature B.V. 2020 P. Vidhyasekaran, Plant Innate Immunity Signals and Signaling Systems, Signaling and Communication in Plants, https://doi.org/10.1007/978-94-024-1940-5_5

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acquired resistance (SAR). NPR1 directly binds SA and activates SA signaling system. NPR1 gene cloned from Arabidopsis thaliana has been used to develop several transgenic crop plants including rice, tomato, citrus, carrot, and strawberry. NPR1like genes isolated from rice, grapevine, apple and tobacco have also been utilized to develop disease-resistant transgenic plants. NPR1 gene expression can be enhanced by treatment with some synthetic chemicals. BTH (benzo[1,2,3]thiadiazole-7carbothioic acid S-methyl ester) is the most successfully developed commercial compound to activate plant innate immune system by enhancing NPR1 gene expression. BTH treatment induces NPR1 mRNA accumulation by several-fold. BTH may also contribute to the establishment of SAR through an interaction with methyl salicylate esterase that is critical for the perception of defense-inducing signals in systemic tissues. Treatment of plants with BTH, which triggers SA signaling, causes the induction of a unique physiological state called “priming”. BTH induces histone modifications, which may be involved in the gene priming.The expression of the WRKY genes is enhanced in BTH-treated plants. BTH triggers NPR1-dependent chromatin modification on WRKY promoters to activate defense gene expression. BTH activates SA-dependent SAR in many crops and has been found to be useful in management of several crop diseases caused by oomyctes, fungi, bacteria, and viruses. N-cyanomethyl-2-chloroisonicotinamide (NCI) is another potential chemical that activates NPR1-dependent SA signaling system. NCI activates SAR by stimulating the site between SA and NPR1. 3-chloro-1-methyl-1H-pyrazole-5-carboxylic acid (CMPA) activates NPR1 in SA signaling pathway. CMPA acts downstream of SA accumulation and acts in the SA signaling pathway between SA production and NPR1 activity. It protects rice from infection by rice blast pathogen Magnaporthe oryzae and bacterial blight pathogen Xanthomonas oryzae pv. oryzae It enhances resistance of tobacco to Pseudomonas syringae pv. tabaci and Oidium sp. Tiadinil (3,4-dichloro-N-(2-cyanophenyl)-1,2-thiazole-5-carboxamide) is another potential chemical, which triggers SA signaling pathway by activating NPR1 gene expression. Tiadinil induces resistance against various fungal, bacterial, and viral diseases in tobacco and is practically used to control rice blast disease. SV-03 is a metabolite of Tiadinil. It stimulates SA signaling pathway downstream of SA production and triggers resistance against various viral, bacterial and fungal pathogens. Probenazole (3-allyloxy-1,2-benzisothiazole-1,1-dioxide) and its metabolite 1,2-benzisothiazole3 (2H)-one 1,1-dioxide (BIT, saccharin) are potential plant defense activators and both of them are known to induce SA accumulation and activate SA signaling system. Probenazole/BIT intervenes in SA signaling system at SA accumulation stage as well as at NPR1 stage to trigger resistance against pathogens. The nonprotein amino acid β-aminobutyric acid (BABA) induces broad-spectrum resistance in a range of crops. BABA induces priming in the SAR induction pathway. The descendants of primed plants exhibit next-generation systemic acquired resistance. SA signaling system can also be activated using plant-derived products. Azelaic acid, a natural compound found in several plants is a signal molecule triggering plant defense responses. Azelaic acid does not directly induce defense responses, but confers on the plants the ability to mount a faster and stronger defense response if and when the plant is

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attacked again. It does this by increasing the production of SA. Azelaic acid stimulates the production of AZ11, a protein which helps prime the plant to build up its immunity by generating additional SA. 3-acetonyl-3-hydroxyoxindole (AHO), isolated from the extracts of Strobilanthes cusia is an activator of SA signaling system. When tobacco plants are treated with AHO, SA accumulates in the leaf tissues and induces disease resistance. An oligosaccharide product obtained from burdock (Arctium lappa) plant triggers production of methyl salicylate involved in SA signaling system and confers disease resistance. N-Acyl-L-homoserine lactones (AHLs)–producing bacteria, which induce SA-dependent systemic resistance, have been shown to be potential tools for management of crop diseases. Some of the rhizobacterial strains activate the plant innate immune system by triggering SA signaling system and they are widely used for management of crop diseases. SA signaling system can be activated by some MAMPs (for Microbe-associated molecular patterns) for effective crop disease management. The MAMP yeast elicitor treatment activates SA signaling system and induces resistance against oomycete, fungal, and bacterial pathogens in many crop plants. Keywords Isochorismate synthase (ICS) · Isochorismate pyruvate lyase (IPL) · Transgenic plants expressing ICS and IPL genes · PAD4 · SID1 · SID2 · RNA-binding protein (RBP) gene · Calmodulin binding protein (CBP) gene · Ubiquitin ligase · NPR1 · BTH · Priming · SAR · NCI · CMPA · Tiadinil · Probenazole · BABA · Azelaic acid · AHO · Rhizobacteria · Yeast elicitor

5.1 Salicylic Acid Signaling System Activates Local Resistance, Systemic Acquired Resistance, and Transgenerational Systemic Disease Resistance Salicylic acid (SA) signaling system is the most important signalng system activating plant innate immunity (Vidhyasekaran 2014, 2015, 2016). This system involves SA biosynthesis (Argueso et al. 2012; Fu et al. 2012; Denancé et al. 2013; GimenezIbanez and Solano 2013; Yang et al. 2013; Tian et al. 2015; Vidhyasekaran 2015; Cueto-Ginzo et al. 2016; Ding et al. 2016; Klessig et al. 2016; Chandrasekhar et al. 2017), reactive oxygen species (ROS) (Chen et al. 1993; LeÒn et al. 1995), MAP kinases (Petersen et al. 2000; Shen et al. 2010), NPR1 (Kesarwani et al. 2007; Tada et al. 2008; Chern et al. 2008), ubiquitin-proteasome system (Vidhyasekaran 2014), nuclear chromatin remodeling (van Den Burg and Takken 2010) and defense gene transcription (Vidhyasekaran 2015). SA signaling system activates not only local resistance, but also systemic acquired resistance (SAR) observed in distal (systemic) tissues (Liu et al. 2011a, b; Du et al. 2012; Shah and Zeier 2013; Vidhyasekaran 2015). SAR is a SA-dependent heightened defense to a broad spectrum of pathogens that is activated throughout a plant following local infection (Liu et al. 2011a). SA signaling causes the induction of a unique physiological state called “priming” (Conrath et al. 2002; Slaughter et al.

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2012). The priming results in a faster and stronger induction of defense mechanisms after pathogen attack (Conrath 2011; Po-Wen et al. 2013). The priming can be inherited epigenetically from disease-exposed plants (Pastor et al. 2013; Vidhyasekaran 2015) and descendants of primed plants exhibit next-generation systemic acquired resistance (Slaughter et al. 2012; Luna et al. 2012). The transgenerational SA-induced SAR has also been reported (Luna et al. 2012; Pieterse 2012).

5.2 Bioengineering Genes to Trigger SA Biosynthesis and Accumulation for Crop Disease Management 5.2.1 Bioengineering Genes Encoding Enzymes Involved in SA Biosynthesis Plants do not have much endogenous SA (Spletzer and Enyedi 1999; Fabro et al. 2008; Vidhyasekaran 2015). It has been suggested that by increasing the SA content, defense genes can be activated and diseases can be controlled (Verberne et al. 2000). Increased synthesis and accumulation of salicylic acid in plants result in increased expression of defense genes conferring resistance against pathogens (Spletzer and Enyedi 1999; Vasiukova and Ozeretskovskaia 2007). SA may be synthesized through the isochorismate pathway (Wildermuth et al. 2001; Gaille et al. 2003; Catinot et al. 2008; Chen et al. 2009; Vidhyasekaran 2015). Isochorismate synthase (ICS) and isochorismate pyruvate lyase (IPL) are the key enzymes involved in biosynthesis of SA (Garcion et al. 2008). SA is synthesized from chorismate, the end product of the shikimate pathway. Chorismate is converted by ICS to isochorismate, which is subsequently cleaved by IPL to yield SA (Verberne et al. 2000). The genes encoding ICS and IPL cloned from two different bacteria have been exploited to develop disease-resistant plants by triggering SA accumulation in tobacco plants (Verberne et al. 2000). To exploit ICS gene, the plastid targeting sequence of the small subunit of tobacco ribulose bisphosphate carboxylase precursor was fused to the ICS coding sequence of the Escherichia coli entC gene. The IPL gene was constructed using the pmsB coding sequence from Pseudomonas fluorescens. The resulting genes, cloned behind the constitutive 35S promoter from Cauliflower mosaic virus were used to transform tobacco plants (Verberne et al. 2000). Transgenic tobacco plants expressing single- gene constructs did not show any increase in accumulation of SA. However, transgenic tobacco plants expressing both ICS and IPL genes showed high increase in SA accumulation (Fig. 5.1; Verberne et al. 2000). The results suggest that for efficient production of SA both ICS and IPL need to be present in the chloroplast, where the highest chorismic acid levels are available. These transgenic plants expressing both the genes alone showed enhanced disease resistance against Tobacco mosaic virus and against the powdery mildew pathogen Oidium lycopersici (Verberne et al. 2000). It appears to be a potential approach to develop disease-resistant plants using SA biosynthesis enzymes.

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Chorismate Bacterial ICS (Isochorismate synthase) gene

Overexpression of ICS

Isochorismate

Bacterial IPL (Isochorismate pyruvate lyase) gene

Overexpression of IPL

Enhanced production of salicylic acid

High increase in SA accumulation

Enhanced disease resistance in transgenic plants expressing both ICS and IPL genes Fig. 5.1 Transgenic tobacco plants overexpressing both ICS and IPL bacterial genes show overproduction of SA (Adapted from Verberne et al. 2000)

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5.2.2 Engineering SA Signaling Regulator Protein Genes Involved in SA Production for Crop Disease Management Several SA signaling regulator proteins are involved in SA production pathway (Vidhyasekaran 2015). SA biosynthesis pathway consists of a linear pathway in which EDS1 (Enhanced Disease Susceptibility1), PAD4 (Phytoalexin Deficient4) and EDS4 activate EDS5/SID1and SID2, which produce SA in Arabidopsis (Glazebrook et al. 2003; Fig. 5.2). EDS1 is required for SA production and it controls SA production to amplify defense signals (Rustérucci et al. 2001; Eulgem et al. 2004). PAD4 is a key regulator acting at upstream of SA (Lippok et al. 2007). EDS1 cooperates closely with PAD4 gene in stimulating production of SA (Zhou et al. 1998; Feys et al. 2001; Glazebrook et al. 2003; Tsuda et al. 2009; Rietz et al. 2011; Makandar et al. 2015; Vidhyasekaran 2015). PAD4 is required for amplification of weak signals to a level sufficient for activation of SA signaling (Jirage et al. 1999). The PAD4 protein sequence displays similarity to triacyl glycerol lipases and other esterases (Jirage et al. 1999). EDS1 heterodimerizes with PAD4 and their nuclear localization is important for subsequent steps in the immune signaling pathway (Feys et al. 2001). EDS1 interacts with another regulator protein, SAG101 (Senescence Associated Gene 101) (Rietz et al. 2011). EDS1 forms several molecularly and spatially distinct complexes with PAD4 and SAG101 (for Senescence associated gene 101) (Wiermer et al. 2005; Xing and Chen 2006). Fig. 5.2 SA signaling regulator proteins involved in SA production (Adapted from Glazebrook et al. 2003; Makandar et al. 2015)

EDS1

PAD4 EDS4

SAG101

SID2

EDS5

SA accumulation

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SID2 is an isochorismate synthase that is involved in biosynthesis of SA (Wildermuth et al. 2001; Vidhyasekaran 2015). SID2 is involved in biosynthesis of SA through isochorismate pathway. Another gene EDS5/SID1 encodes a protein, which transports precursors for SA biosynthesis. EDS5 exhibits homology to multidrug and toxin extrusion (MATE) transporter proteins from animals (Nawrath et al. 2002). EDS5 expression requires PAD4, placing EDS5 downstream of PAD4 (Nawrath et al. 2002). EDS4 plays a role in SA signaling and in SA-induced systemic acquired resistance (Gupta et al. 2000). The eds4 mutant plants showed reduced accumulation of SA induced by Pseudomonas syringae pv. maculicola infection (Gupta et al. 2000). SAG101 contributes to the SA accumulation in Arabidopsis (Makandar et al. 2015). PAD4 gene has been exploited to develop disease-resistant wheat plants (Makandar et al. 2015). Transgenic wheat plants overexpressing the Arabidopsis PAD4 coding sequence were developed. The maize ubiquitin (ubi) gene promoter was used to drive expression of PAD4. Constitutive expression of PAD4 resulted in significantly higher basal and Fusarium gramineum infection-induced accumulation of SA in the spikes of transgenic wheat lines than in nontransgenic plants. The higher accumulation of SA in the transgenic plants was accompanied by enhanced resistance against the Fusarium head blight (FHB) pathogen F. graminearum. FHB disease severity was significantly lower on spikes of the transgenic plants (Makandar et al. 2015). The results suggest that improving the ability of wheat spikes to accumulate SA is potentially attractive strategy for the FHB disease management in wheat (Makandar et al. 2015). EDR2 (ENHANCED DISEASE RESISTANCE2) negatively regulates SAbased defense response against the powdery mildew pathogen Golovinomyces cichoracearum (Vorwerk et al. 2007). Loss-of-function mutations in EDR2 lead to enhanced resistance against the pathogen (Yao et al. 2012). The results suggest that EDR2 gene can be manipulated to develop disease resistant plants.

5.2.3 Engineering RNA-Binding Protein Gene to Activate SA Biosynthesis Pathway Gene expression in plants is commonly regulated at both transcriptional and posttranscriptional levels (Lorkovic 2009; Huh and Paek 2013a). RNA-binding proteins (RBP) play important roles in post-transcriptional gene regulation by controlling splicing, polyadenylation, mRNA stability, RNA trafficking, and translation (Glisovic et al. 2008; Pallas and Gomez 2013). They act by regulating pre-mRNA splicing, polyadenylation, RNA stability and RNA export, as well as by influencing chromatin modification (Lorkovic 2009). RBPs determine the fate of RNA from synthesis to decay (Marondedze et al. 2016). After protein-coding genes are transcribed into premRNA by RNA polymerase II, processing and modification steps, such as splicing, are required to produce functional mRNA that is ready for export from the nucleus to the cytoplasm. The cytoplasmic mRNAs can be translated or degraded. RBP can

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regulate all of these processes (Lorkovic 2009). Plant RBPs are characterized by the presence of RNA-binding domains, such as the RNA recognition motif (RRM), the K-Homology (KH) domain, Pumilio/FBF (PUF) domain, and double-stranded RNA binding domain (DS-RBD) (Lunde et al. 2007; Lorkovic 2009; Quenault et al. 2011; Huh and Paek 2013b; Lee and Kang 2016). Many RBPs have been shown to be involved in plant innate immunity (Fu et al. 2007; Zhu et al. 2007; Fujisaki and Ishikawa 2008; Qi et al. 2010; Lee et al. 2012a, b; Huh et al. 2013; Huh and Paek 2013a; Staiger et al. 2013). A RBP from Arabidopsis thaliana, AtRBP-defense related 1 (AtRBP-DR1), has been shown to be involved in plant immune responses (Qi et al. 2010). The AtRBPDR1 gene was cloned and exploited for developing disease-resistant plants. Transgenic Arabidopsis plants overexpressing AtRBP-DR1 were developed (Qi et al. 2010). These transgenic plants showed higher mRNA levels of SID2. The SID2 gene encodes an isochorismate synthase, which is required for producing SA during immune responses (Wildermuth et al. 2001). Activation of the SA pathway by AtRBP-DR1 overexpression was fully dependent on SID2 (Qi et al. 2010). Overexpression of AtRBP-DR1 led to high accumulation of SA and these transgenic plants showed enhanced resistance to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Qi et al. 2010). These studies suggest that the RBP-DR1 gene is a potential tool to develop disease-resistant plants by activating SA biosynthesis pathway (Qi et al. 2010).

5.2.4 Engineering Calmodulin-Binding Protein Gene to Trigger SA Biosynthesis for Disease Management Calcium signaling system has been shown to be involved in triggering SA biosynthesis pathway (Vidhyasekaran 2014, 2015, 2016). The calcium signature is perceived by different Ca2+ -binding proteins (Kudla et al. 2010). Ca2+ signaling pathways are composed of molecular relays; the first runner after Ca2+ is Ca2+ “sensor” (Snedden and Fromm 2001). Calmodulin (CaM) is an important Ca2+ sensor (Reddy et al. 2011a). It binds to a variety of proteins involved in various signaling systems triggering defense responses (van Verk et al. 2011). A camodulin binding protein, CBP60g, has been shown to be involved in activating SA biosynthesis (Wang et al. 2009). CBP60g has been shown to participate in SA signaling biosynthesis and accumulation (Wang et al. 2009). It has been suggested that the signal coming from CBP60g may act upstream from SA synthesis (Wang et al. 2009). It may activate PAD4, a key regulator in the SA biosynthesis pathway (Zhou et al. 1998; Lippok et al. 2007; Tsuda et al. 2008; Wang et al. 2009). PAD4 is required for amplification of weak signals to a level sufficient for activation of SA signaling (Jirage et al. 1999). Downstream of PAD4, CBP60g may act upstream of SID2, an isochorismate synthase that is involved in biosynthesis of SA (Wang et al. 2009, 2011). Isochorismate synthase encoded by SID2 is essential for the

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biosynthesis of salicylic acid (Garcion et al. 2008; Truman and Glazebrook 2012). The calmodulin binding protein CBP60g has been shown to bind to the promoter region of SID2 (Zhang et al. 2010b). A central domain of CBP60g was found to bind to an oligomer with the sequence GAAATTTTGG selected from the SID2 promoter (Zhang et al. 2010b). CBP60g shows DNA binding activity, and it preferentially binds to a DNA sequence that contains AATTTT, which is present in the promoter of ICS1 (Fig. 5.3; Wang et al. 2011). Transgenic Arabidopsis plants overexpressing CBP60g gene were developed and these transgenic plants showed elevated SA accumulation and increased expression of the defense genes (Wan et al. 2012). The transgenic plants showed enhanced resistance against the bacterial pathogen Pseudomonas syringae Calmodulin-binding protein CBP60g

activation

PAD4

Binding of CBP60g to the promoter of SID2 gene

Increased expression of SID2 gene

Increased activity of isochorismate synthase (ICS)

Increased accumulation of SA

Increased defense responses

Fig. 5.3 Engineering a calmodulin-binding protein gene to trigger SA accumulation (Adapted from Wang et al. 2011; Wan et al. 2012)

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(Wan et al. 2012). The results suggest that engineering the calmodulin-binding protein gene may be a potential approach for developing disease-resistant plants.

5.2.5 Engineering WRKY Transcription Factor Genes to Activate SA Biosynthesis Genes for Crop Disease Management Transcription factors are the master regulators of expression of genes involved in plant innate immune signaling systems. Transcription factors regulate the gene transcription processes by modulating the rate of transcription initiation of target genes (Du et al. 2009). Several transcription factors are known to take part in the regulation of SA signaling pathway (Maleck et al. 2000; Després et al. 2003; Li et al. 2004; Kim et al. 2007; Raffaele et al. 2006; Waller et al. 2006; Wang et al. 2006; Zheng et al. 2006; Nobuta et al. 2007; Zheng et al. 2007; Xing et al. 2008; Seo and Park 2010; van Verk et al. 2011; Hu et al. 2012; Takatsuji et al. 2014; Vidhyasekaran 2015). One of the rice WRKY genes, OsWRKY13, showed increased expression after incompatible pathogen infection in several rice lines conferring resistance to the rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae and the rice blast pathogen Magnaporthe grisea. However, there was no change in expression of OsWRKY13 gene in compatible interactions (Wen et al. 2003). It suggests that increased expression of OsWRKY13 may induce resistance against diseases caused by various pathogens. The OsWRKY13 gene was cloned and transgenic rice plants overexpressing the gene were developed (Qiu et al. 2007; Vidhyasekaran 2016). The transgenic plants accumulated significantly more PAD4 (phytoalexin-deficient 4) than did the wildtype plants (Qiu et al. 2007). PAD4 is a key regulator of SA biosynthesis pathway and it acts upstream of SA (Lippok et al. 2007). It has been suggested that PAD4 transduces ROS-derived signals leading to SA production (Mateo et al. 2004; Wiermer et al. 2005). PAD4 is required for amplification of weak signals to a level sufficient for activation of SA signaling (Jirage et al. 1999). The PAD4 protein sequence displays similarity to triacyl glycerol lipases and other esterases (Jirage et al. 1999). The OsWRKY13-overexpressing plants accumulated significantly more ICS1 (isochorismate synthase 1) and ICS plays an important role in SA biosynthesis via isochorismate pathway (Garcion et al. 2008). The transgenic plants also showed accumulation of free salicylic acid (Qiu et al. 2007; Vidhyasekaran 2016). These results suggest that the transgene OsWRKY13 triggers SA biosynthesis pathway. Transgenic rice plants overexpressing OsWRKY13 showed reduced blast disease incidence (Cheng et al. 2015). The transgenic rice plants overexpressing OsWRKY13 showed enhanced resistance to the rice blast pathogen M. oryzae both under greenhouse and field conditions (Qiu et al. 2007). These transgenic plants also showed resistance to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae. When these transgenic plants were inoculated with the bacterial pathogen, growth rate of the bacteria on the plants was 5.5 to 13.9-fold lower than that on wild-type plants. The

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lesion area on the bacteria-infected leaves was also reduced in the transgenic plants. The OsWRKY13 gene conferred resistance against both the bacterial and fungal diseases at both seedling and adult stages in rice without causing any deleterious effects (Qiu et al. 2007). These studies indicate that OsWRKY13 provides a transgenic tool for engineering wide-spectrum disease resistance in rice. Another WRKY gene, OsWRKY89 was found to play an important role in triggering SA accumulation and activating defense responses against the rice blast pathogen M. oryzae (Wang et al. 2007; Vidhyasekaran 2016). Transgenic rice plants overexpressing OsWRKY89 were developed and these transgenic plants showed an increase in SA levels. These transgenic plants showed enhanced resistance to the blast pathogen M. oryzae (Wang et al. 2007). These results suggest that OsWRKY89 is another potential transcription factor which can be exploited to develop disease resistant plants.

5.2.6 Engineering Gene Encoding WIPK-Activated Transcription Factor to Increase Accumulation of SA for Crop Disease Management NtWIF (Nicotiana tabacum WIPK-interacting factor), a transcription factor activated upon phosphorylation by wound-induced protein kinase (WIPK) has been exploited to develop disease resistant tobacco plants (Waller et al. 2006; Vidhyasekaran 2016). NtWIF is a 648 amino acid protein possessing the N-terminal DNA-binding B3 domain, the middle transactivation domain and the C-terminal WIPK—interacting domain. Upon binding to WIPK, the N-terminal region is phosphorylated. Transgenic tobacco plants overexpressing NtWIF were developed. The transgenic plants contained more than 50-fold higher SA levels than the wild-type plants (Fig. 5.4; Waller et al. 2006). The transgenic plants showed increased resistance against Tobacco mosaic virus (Fig. 5.5; Waller et al. 2006). The results suggest that the NtWIF gene can be exploited for effective management of an important viral disease in tobacco.

5.2.7 Engineering Ubiquitin-Proteasome Pathway Genes to Trigger SA Accumulation for Crop Disease Management Ubiquitin- and proteasome-mediated degradation of proteins plays an important role in plant defense signaling system (Lee et al. 2011; Li et al. 2011; Sahana et al. 2012; Yao and Ndoja 2012; Vidhyasekaran 2014). Proteasomes are large protein complexes located in the nucleus and the cytoplasm (Peters et al. 1994). The main function of the proteasome is to degrade unneeded or damaged proteins by proteolysis. Proteasomes regulate the concentration of particular proteins and degrade misfolded proteins.

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Salicylic acid (n mol per g fresh wt)

8 6 4 2 0 Wild-type plant

Transgenic plant

Fig. 5.4 Increase in salicylic acid content in transgenic tobacco plants overexpressing NtWIF when exposed to stress (Adapted from Waller et al. 2006) 4.5 4 3.5 3 2.5 Lesion size (mm) 2 1.5 1 0.5 0 Wild-type plants

Transgenic plants

Fig. 5.5 Transgenic tobacco plants expressing NtWIF gene show enhanced resistance against Tobacco mosaic virus (Adapted from Waller et al. 2006)

Proteins are tagged for degradation by a small protein called ubiquitin (Pickart and Eddins 2004). Ubiquitin contains 76 amino acids and it is covalently conjugated to Lys residues in substrate proteins (Dreher and Callis 2007). Proteins are targeted for degradation by the proteasome by covalent modification of a lysine residue that requires the coordinated reactions of three enzymes. In the first step, a ubiquitin-activating enzyme, E1, activates ubiquitin C-terminal carboxyl group by adenylation, and then forms a thioester bond with cysteinyl sulfhydryl residue on the E1 protein itself (Lee et al. 2011). The adenylated ubiquitin is then transferred to a cysteine of the second enzyme, ubiquitin-conjugating enzyme (E2). A member of a highly diverse class of enzymes known as ubiquitin ligases (E3)

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recognizes the specific protein to be ubiquitinated and catalyzes the transfer of ubiquitin from E2 to this target protein (Pickart and Eddins 2004; Smalle and Vierstra 2004; Dreher and Callis 2007). A target protein must be labeled with at least four ubiquitin monomers in the form of a polyubiquitin chain before it is recognized by the proteasome lid (Thrower et al. 2000). Ubiquitin-ubiquitin linkages may serve as proteolytic signals (Kirkpatrick et al. 2006). E3 ubiquitin ligases play a key role in the ubiquitin-proteasome system (UPS). E3 ubiquitin ligases are classified into two groups based on the presence of a HECT (for Homologous to E6-AP COOH Terminus) or RING (for Really Interesting New Gene)/U box domain (Zheng et al. 2000; Pickart 2001; Andersen et al. 2004). Several proteins containing U-box and RING domains have been reported in plants (Stone et al. 2005). The RING domain has a consensus sequence containing Cys and His residues (Cys-X2 -Cys-X9–39 -Cys-X1–3 -His-X2–3 -Cys/His-X2 -CysX4–48 -Cys-X2 -Cys) (Lee et al. 2011). Based on the presence of Cys or His in the fifth position, the RING domains of RING finger type proteins can be divided into two types, C3-H-C4 and C3-H2-C3 (Borden and Freemont 1996). Plants contain several RING-type E3 ubiquitin ligases and more than 400 RING-type proteins have been reported in Arabidopsis thaliana (Stone et al. 2005). Ubiquitination is a unique posttranslational modification system that has been shown to play a significant role in the recognition and induction of various signals by modulating the stability of proteins involved in signal perception or responses (Smalle and Vierstra 2004; Dreher and Callis 2007; Lee et al. 2011; Vidhyasekaran 2014). The pepper E3 ubiquitin ligase RING1 gene, CaRING1, has been shown to regulate SA accumulation in pepper plants (Lee et al. 2011). Virus-induced gene silencing of CaRING1 lowered SA levels in pepper plants. Silencing of CaRING1 conferred enhanced susceptibility to avirulent Xanthomonas campestris pv. vesicatoria infection accompanied by reduced expression of SA-dependent PR-1 gene expression in pepper plants (Lee et al. 2011). The results suggest that the CaRING1 gene can be exploited to manipulate SA accumulation and trigger SA signaling system to manage crop diseases. The usefulness of the CaRING1 gene for disease management has been demonstrated in the model weed plant Arabidopsis thaliana. Transgenic Arabidopsis plants expressing the pepper CaRING1 gene were developed (Lee et al. 2011). Overexpression of CaRING1 gene in A. thaliana showed enhanced accumulation of SA. Overexpression of CaRING1 in A. thaliana conferred enhanced resistance to the bacterial pathogen Pseudomonas syringae pv. tomato and to the oomycete pathogen Hyaloperonospora arabidopsidis infections. These results suggest that the CaRING1 positively regulates SA accumulation and SA-mediated defense responses and can be exploited for developing disease resistant plants. A cDNA clone (OsRHC1), which encodes a RING zinc finger protein, was obtained (Cheung et al. 2007). OsRHC1 was found to be localized on plasma membrane of rice cells. Transgenic Arabidopsis plants expressing the rice OsRHC1 gene showed enhanced resistance against Pseudomonas syringae pv. tomato. The protective effect in the transgenic plants was neutralized in an npr1 mutation background

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(Cheung et al. 2007). The results suggest that NPR1 plays important role in conferring resistance against the bacterial pathogen and OsRHC1 is a potential gene to develop disease-resistant plants. Protein degradation through ubiquitin-proteasome pathway plays an important role in defense signaling. However, some of these pathways may act as negative regulators of defense signaling (Conrath et al. 1998; Kim and Delaney 2002; Vidhyasekaran 2014). These negative regulators of defense signaling systems were also exploited to develop disease-resistant plants (Conrath et al. 1998). A variant ubiquitin in which Lys48 (the site of branch formation) is replaced by Arg (ubr48), does not support proteolytic degradation of model substrates in an in vitro system, but allows monoubiquitination to occur at roughly wild-type rates (Chau et al. 1989). This ubiquitin variant, ubR48, acts as a specific inhibitor of ubiquitin-dependent proteolysis (Becker et al. 1993). Transgenic tobacco plants expressing a ubiquitinvariant with Lys to Arg exchange in position 48 (ubr48) were developed (Becker et al. 1993). These transgenic tobacco plants showed enhanced resistance against Tobacco mosaic virus (Becker et al. 1993). The transgenic plants expressing the ubiquitin variant ubr78 contained elevated levels of SA compared to the control plants (Fig. 5.6; Conrath et al. 1998). Accumulation of salicylic acid coincided with high levels of PR1 protein. These transgenic plants showed accumulation of callose and enhanced resistance to Tobacco mosaic virus (Conrath et al. 1998). The results suggest that ubiquitin-proteasome pathway can be manipulated to trigger SA signaling system for crop disease management. SGT1 (for Suppressor of the G2 allele of SKP1) associates with SKP1, a component of the SCF-type E3 complexes (Kitagawa et al. 1999; Liu et al. 2002; Peart et al. 2002). SGT1 plays key role in ubiquitin-proteasome-mediated proteolytic pathway (Seo et al. 2008). SGT1 is involved in basal defense response besides effector triggered immunity (ETI). Silencing GmSGT1-2 impaired resistance to virulent bacterial pathogens and systemic acquired resistance (SAR) in soybean (Fu et al. 2009). 0.7 0.6 0.5 0.4

Salicylic acid (μg/g)

0.3 0.2 0.1 0

Control plants

Transgenic plants

Fig. 5.6 Endogenous levels of SA in transgenic tobacco plants expressing ubr48 gene (Adapted from Conrath et al. 1998)

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14 12 10

Lesion length (cm)

8 6 4 2 0 Wild-type plants

OsSGT1 overexpressing transgenic plants

Fig. 5.7 Transgenic rice plants overexpressing OsSGT1 show enhanced resistance against the rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Adapted from Wang et al. 2008)

SGT1 genes have been shown to be required for SA accumulation in Arabidopsis for induction of disease resistance (Zhou et al. 2008). The usefulness of SGT1 gene in developing transgenic plants for control of crop diseases was assessed (Wang et al. 2008). Transgenic rice plants constitutively expressing the OsSGT1 gene were generated. The transgenic plants exhibited enhanced resistance to the blast fungus Magnaporthe oryzae. The transgenic plants showed enhanced resistance to all the tested four races of the pathogen. The transgenic plants overexpressing OsSGT1 also showed enhanced resistance to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Wang et al. 2008; Fig. 5.7). The results suggest that SGT1 is a potential gene which can be engineered to develop disease-resistant plants by activating SA biosynthesis.

5.3 Bioengineering NPR1 Genes for Crop Disease Management 5.3.1 NPR1 Is a Key Component in SA-Triggered SAR SA is an endogenous plant hormone signal essential to the development of a long-lasting broad-based immunity called systemic acquired resistance (SAR) (Vidhyasekaran 2015; Withers and Dong 2016). NPR1 (for non-expressor of PR gene1; also known as NIM1 [nonimmunity1] and SAI1 [salicylic acid inducible1]) gene is a master regulator of the SA-mediated induction of SAR (Durrant and Dong 2004; Lin et al. 2004; Maier et al. 2011; Pieterse 2012; Hermann et al. 2013; Lee et al. 2015; Kuai et al. 2015; Saleh et al. 2015; Vidhyasekaran 2015). NPR1 is an important

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regulator of responses downstream of SA (Mou et al. 2003; Chern et al. 2008; Zhang et al. 2003a). NPR1 expression levels become elevated upon induction by SA (Cao et al. 1997). NPR1 gene is a master regulator of the SA-mediated induction of defense genes (Mou et al. 2003; Zhang et al. 2003a; Chern et al. 2008). NPR1 directly binds SA (Wu et al. 2012; Kuai et al. 2015) and activates SA signaling system. Nuclear localization of NPR1 protein has been shown to be essential for its function (Kinkema et al. 2000; Meur et al. 2006; Vidhyasekaran 2015). In the unstressed healthy plants, NPR1 is retained in the cytoplasm. Without induction, NPR1 protein forms an oligomer and is excluded from the nucleus. When the plants are stressed, SA accumulates in the stressed plants (Durrant and Dong 2004). The induced SA controls the nuclear translocation of NPR1 (Spoel and Dong 2012). NPR1 is sequestered in the cytoplasm as an oligomer through intermolecular disulfide bonds. After induction by SA, the disulphide bonds are reduced, releasing NPR1 monomers into the nucleus (Kinkema et al. 2000; Mou et al. 2003). SA regulates the conversion of NPR1 from an oligomeric to monomeric form, which leads to its nuclear location (Tada et al. 2008). A canonical DNA-binding domain is absent in NPR1. It regulates PR gene expression as a cofactor of the TGA transcription factors, which interact with NPR1 (Fan and Dong 2002; Kesarwani et al. 2007). NPR1 enhances the binding of TGA factors to the promoter of PR genes (Johnson et al. 2003, 2008). TGA factors bind to the as-1 (cis-acting) element of the PR promoter (Johnson et al. 2003; Rochon et al. 2006). NPR1 may transiently interact with the DNA unbound fraction of TGA to promote its recruitment to an active form on cognate target promoters (Johnson et al. 2008).

5.3.2 Engineering Arabidopsis NPR1 Gene in Crop Plants for Disease Management Several studies have shown that NPR1 may not be active in healthy unstressed plants to trigger SA downstream signaling system. Engineering the NPR1 gene to constitutively overexpress in plants may be a potential approach to trigger SA signaling system and enhance the defense gene expression for crop disease management (Vidhyasekaran 2015). NPR1 gene cloned from Arabidopsis thaliana has been used to develop several transgenic crop plants (Lin et al. 2004; Wally et al. 2009; Zhang et al. 2010a; Kumar et al. 2013; Dutt et al. 2015; Silva et al. 2015). Sweet orange trees expressing an A. thaliana NPR1 gene under the control of a constitutive CaMV 35S promoter were developed (Dutt et al. 2015). The selected transgenic lines had one to three copies of NPR1 gene integrated into the citrus genome and the lines varied in the degree of expression of NPR1. The lines which showed high NPR1 gene expression showed higher expression of SA signaling pathway dependent PR-1 gene expression compared to the line showing lesser expression of NPR1. In control plants expression of NPR1 and PR-1 genes could be detected (Dutt et al. 2015). The

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results suggest that overexpression of NPR1 gene results in activation of SA signaling system, ultimately leading to high expression of the defense-related PR-1 gene. The transgenic citrus plants overexpressing AtNPR1 showed enhanced resistance to Citrus Huanglongbing (Citrus greening) disease caused by the phloem-limited bacterium Candidatus Liberibacter asiaticus, which is spread by the Asian citrus psyllid vector, Diaphorina citri (Dutt et al. 2015). Overexpression of AtNPR1 resulted in trees with normal phenotypes that exhibited enhanced resistance to the bacterial disease. Transgenic trees exhibited reduced disease severity and a few lines remained disease-free even after 36 months of planting in a high-disease pressure field site (Dutt et al. 2015). It has been suggested that AtNPR1 gene being plant-derived can serve as a component for the development of consumer friendly genetically modified citrus trees for disease management. Citrus canker is another important disease caused by Xanthomonas citri subsp. citri affecting several Citrus species. Effective and economically viable control measues against the disease are not yet available. Arabidopsis NPR1 gene was employed to develop transgenic citrus plants overexpressing the transgene (Zhang et al. 2010a). Overexpression of AtNPR1 in citrus increased resistance to the canker diease and the resistance was related with the expression levels of AtNPR1 in the transgenic plants. The line with the highest expression level of AtNPR1 was also the most resistant.The results suggest overexpression of AtNPR1 in citrus is a promising approach for development of resistant cultivars to citrus canker (Zhang et al. 2010a). Transgenic sweet orange plants overexpressing the Arabidopsis NPR1 gene were also produced (Boscariol-Camargo et al. 2016). The transgenic plants showed stronger expression of EDS1 after pathogen inoculation. EDS1 is a regulatory protein required for SA production and it controls SA production to amplify defense signals (Feys et al. 2001; Rustérucci et al. 2001; Eulgem et al. 2004). These transgenic plants showed resistance against the bacterial pathogen X. citri subsp. citri. The leaves of these transgenic plants exhibited fewer lesions and reduced bacterial concentrations compared to non-transformed control (Boscariol-Camargo et al. 2016). Arabidopsis NPR1 gene has been exploited to develop transgenic tomato plants overexpressing AtNPR1 (Lin et al. 2004). These transgenis plants showed enhanced resistance against a spectrum of fungal and bacterial diseases including fusarium wilt (Fusarium oxysporum f. sp. lycopersici), bacterial wilt (Ralstonia solanacearum), gray leaf spot (Stemphylium spp.) and bacterial spot (Xanthomonas vesicatoria). Transgenic lines that accumulated higher levels of NPR1 proteins exhibited higher levels and a broader spectrum of enhanced resistance to the diseases. Further, the enhanced disease-resistance was stably inherited (Lin et al. 2004). The overexpression of the SAR controlling master switch, NPR1, in carrot tissues offers the ability to control a wide range of different pathogens in carrot (Wally et al. 2009). The Arabidopsis NPR1 gene was introduced into carrot under control of CaMV 35S promoter. The transgenic carrot plants showed enhanced resistance against the powdery mildew pathogen Erysiphe heraclei, the bacterial pathogen Xanthomonas hortorum and the necrotropic fungal pathogens Alternaria radicina, Botrytis cinerea and Sclerotinia sclerotiorum (Wally et al. 2009).

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Leaf lesion size 0.8 (Cm2) 0.6 0.4 0.2 0 Wild-type plants

Transgenic plants

Fig. 5.8 Transgenic rice plants expressing AtNPR1 gene show enhanced resistance against Magnaporthe oryzae (Adapted from Quilis et al. 2008)

Strawberry is an economically important fruit crop worldwide and affected by several diseases. Transgenic strawberry plants expressing Arabidopsis NPR1 gene show enhanced resistance against anthracnose (Colletotrichum fragariae), powdery mildew, and angular leafspot (Xanthomonas fragariae) diseases (Silva et al. 2015). The increased resistance observed in the transgenic plants was found to be related to the relative expression levels of AtNPR1in the transgenic plants (Silva et al. 2015). Transgenic rice plants constitutively expressing the Arabidopsis NPR1 gene were developed. These transgenic plants showed resistance against the rice blast pathogen Magnaporthe oryzae (Fig. 5.8; Quilis et al. 2008). AtNPR1 has been shown to exert its protective effect against M. oryzae by priming the expression of SA-responsive endogenous genes, such as PR1b, PR5, PR10 and PBZ1 (Quilis et al. 2008). Transgenic rice plants expressing the Arabidopsis NPR1 gene also showed resistance against the sheath blight pathogen Rhizoctonia solani (Molla et al. 2016). The elevated levels of NPR1 activated the defense pathway in the transgenic plants by inducing expression of endogenous genes such as PR1b, RC24, and PR10A. The transgenic plants did not exhibit any kind of phenotypic imbalances (Molla et al. 2016). These results suggest that Arabidopsis NPR1 gene can be engineered in rice plants for inducing defense responses against various pathogens without affecting the yield potential of rice plants. Fusarium head blight caused by Fusarium graminearum is a devastating disease of wheat. Transgenic wheat plants expressing the Arabidopsis NPR1 gene were developed and these transgenic plants showed enhanced resistance against the fusarium head blight (Fig. 5.9; Makandar et al. 2006). The resistance observed in the transgenic plants was found to be heritable systemic acquired resistance. The heightened fusarium head blight resistance in the transgenic AtNPR1-expressing wheat was associated with faster activation of defense response when challenged by the pathogen F. graminearum. Expression of the pathogenesis-related protein PR1 was induced rapidly to a high level in the pathogen-challenged spikes of AtNPR1-expressing wheat

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90 80 70 60 50 Infected spikelets (%) 40 30 20 10 0 Contol

Transgenic plants

Fig. 5.9 Transgenic wheat plants overexpressing AtNPR1 show enhanced resistance against Fusarium head blight (Adapted from Makandar et al. 2006)

plants (Makandar et al. 2006). These results suggest that AtNPR1 gene is a potential candidate to develop disease-resistant wheat plants. Transgenic cotton plants expressing Arabidopsis NPR1 gene were also developed. The NPR1-expressing cotton plants exhibited significant resistance to Verticillium dahliae isolate TS2 and Fusarium oxysporum f. sp. vasinfectum (Parkhi et al. 2010b). However, these transgenic plants showed resistance only against some isolates of Verticillium dahliae (Parkhi et al. 2010a), and Fusarium oxysporum f. sp. vasinfectum (Joshi et al. 2017). The transgenic plants also showed resistance against Rhizoctonia solani and Alternaria alternata (Parkhi et al. 2010b). The transgenic cotton plants also showed significant tolerance to the black root rot pathogen Thielaviopsis basicola (Kumar et al. 2013). Although the transformants showed the typical root discoloration symptoms similar to the wild-type control plants following infection, their roots tended to recover faster and resumed normal growth. The Arabidopsis NPR1-overexpressing transgenic plants exhibited stronger and faster induction of defense-related genes (Kumar et al. 2013). These studies show that Arabidopsis NPR1 gene is a potential tool for developing disease-resistant crop plants.

5.3.3 Engineering NPR1-like Genes for Crop Disease Management NPR1 is a key regulator of SA-mediated systemic acquired resistance (SAR) in plants. NPR1 is functionally conserved in diverse plant species (Yuan et al. 2007). Arabidopsis NPR1 has been widely employed to trigger SAR in various plant species for crop disease management (Lin et al. 2004; Makandar et al. 2006; Quilis et al. 2008; Wally et al. 2009; Parkhi et al. 2010b; Zhang et al. 2010a; Kumar et al. 2013; Dutt et al. 2015; Silva et al. 2015; Boscariol-Camargo et al. 2016; Molla et al. 2016;

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Joshi et al. 2017). Search for NPR1-like genes in other plant species has been made to utilize them for activating SAR more effectively in crop plants. Five NPR1-like genes have been identified in rice genome and named as OsNPR1/NH1 (NPR1 Homologue 1), OsNPR2/NH2, OsNPR3, OsNPR4 and OsNPR5 (Chern et al. 2005; Yuan et al. 2007). Among them, OsNPR1 may be the true rice orthologue of Arabidopsis NPR1 (Yuan et al. 2007). Transgenic rice plants over-expressing the OsNPR1 genomic coding region and the full length cDNA were developed. Both genomic DNA and cDNA transgenic lines showed enhanced resistance to the rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Yuan et al. 2007). OsNPR1-mediated disease resistance was displayed with a dose-related manner of transgene expression (Yuan et al. 2007). Transgenic lines over-expressing two other NPR1-like genes, OsNPR2 and OsNPR3 did not show enhanced resistance to X. oryzae pv. oryzae (Yuan et al. 2007). Further localization of OsNPR1 in the nucleus of the transgenic plants seems to be more effective in developing disease-resistant plants. OsNPR1 was found to be localized in the cytoplasm. Treatment with the strong reducing agent dithiothreitol resulted in the movement of OsNPR1 into the nucleus, suggesting that the OsNPR1 oligomer was converted to the monomer by a change in cellular redox potential. The OsNPR1 protein contains two conserved cysteine residues at positions 76 and 216. These two conserved cysteine residues are essential to the formation of the NPR1 oligomer through disulphide bonds. These two cysteine residues were mutated into alanine (C76A+216A). Transgenic rice lines expressing the mutant OsNPR1(2CA) were generated and in these transgenic plants OsNPR1(2CA) was found to be localized in the nucleus (Yuan et al. 2007). The transgenic plants expressing OsNPR1 showed enhanced resistance against X. oryzae pv. oryzae. However OsNPR1 overexpression resulted in increased susceptibility to insect pests (Yuan et al. 2007). This may be due to suppression of JA signaling system by the increased expression of SA signaling system in the transgenic plants. Antagonism between SA and JA signaling pathways has been widely reported in plants (Pieterse et al. 2012; Gimenez-Ibanez and Solano 2013; Van der Does et al. 2013; Vidhyasekaran 2015). The transgenic OsNPR1(2CA) expressing plants showed enhanced resistance against X. oryzae pv. oryzae without any increase in susceptibility to insect pests. Unlike OsNPR1-expressing plants, the JA signaling system was not suppressed in OsNPR1 (2CA) overexpressing plants (Yuan et al. 2007). The results suggest that OsNPR1 (2CA) construct may be more useful in developing disease-resistant plants without any adverse effect of increase in insect pest susceptibility. Chern et al. (2005) isolated a rice NPR1 homologue (NH1, also called OsNPR1) and developed transgenic rice plants overexpressing the NH1gene. The transgenic plants showed high levels of resistance against X. oryzae pv. oryzae (Fig. 5.10; Chern et al. 2005). Feng et al. (2011) developed transgenic rice plants overexpressing OsNPR1 and these transgenic plants showed enhanced resistance against the rice blast pathogen Magnaporthe oryzae (Feng et al. 2011). These transgenic plants showed increased expression of defense-related genes such as PR-1a, PBZ1, CHI, GLU, and PAL genes (Feng et al. 2011).

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25 20 15

Lesion length (cm) 10 5 0 Wild-type plants

Transgenic plants overexpressing NH1 gene

Fig. 5.10 Transgenic rice plants over-expressing NH1 gene show resistance against Xanthomonas oryzae pv. oryzae (Adapted from Chern et al. 2005)

Four rice NPR1 paralogs have been detected in rice genome. Among them rice NPR1 paralog 3 (NH3) was employed for developing disease-resistant rice plants (Bai et al. 2011). Transgenic rice plants overexpressing NH3 were developed using the maize ubiquitin-1 (ubi-1) promoter. The rice NH3 cDNA was introduced into an ubi-C1300-based binary vector to develop the transgenic plants. These transgenic plants did not show any enhanced resistance against the rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae. However, introduction of an extra copy of NH3 driven by its own promoter (nNT-NH3) resulted in enhanced resistance in the transgenic plants. The bacterial population levels were reduced to 10-fold in nNTNH3 transgenic plants compared to control rice plants. The bacterial blight lesion development was also suppressed in these transgenic plants (Bai et al. 2011). These studies suggest that specific NPR1 genes driven by selected promoters will be ideal tools to develop disease-resistant rice plants. Two Arabidopsis NPR1-like genes (VvNPR1.1 and VvNPR1.2) have been isolated from grapevine (Vitis vinifera) and among them VvNPR1.1 is a functional ortholog of AtNPR1, whereas VvNPR1.2 shows different function. Transgenic grapevine plants overexpressing VvNPR.1 showed enhanced resistance against the powdery mildew pathogen (Le Henanff et al. 2011). Stable overexpression of VvNPR1.1 in grapevine resulted in constitutive nuclear localization of the VvNPR1.1 protein and enhanced PR1 gene expression in the transgenic plants (Le Henanff et al. 2011). PR-1 is a SA signaling pathway marker gene (Takahashi et al. 2004; Edgar et al. 2006; Nobuta et al. 2007; Zheng et al. 2007; Xing et al. 2008). Enhanced PR1 gene expression in the VvNPR1.1–overexpressing plants suggests that SA signaling system has been activated in the transgenic plants. An NPR1 homolog, MpNPR1, was cloned from Malus X domestica. Transgenic apple plants overexpressing MpNPR1 were developed. These plants showed enhanced resistance against the fire blight pathogen Erwinia amylovora (Malnoy

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et al. 2006). Another NPR1 homolog, MhNPR1, was isolated from Malus hupehensis and the gene was introduced into ‘Fuji’ apple. The transgenic apple plants showed enhanced resistance against the powdery mildew disease. Overexpression of the MhNPR1 gene induced SAR and enhanced the Fuji apple’s resistance to the powdery mildew disease (Chen et al. 2012). Transgenic tobacco plants overexpressing MhNPR1 gene show enhanced expression of PR genes and enhanced resistance against Botrytis cinerea (Chen et al. 2012). These studies suggest that NPR1 is a potential gene, which can be exploited to develop disease-resistant plants.

5.4 Manipulation of NPR1 Gene Expression by Synthetic Chemicals to Trigger Systemic Acquired Resistance (SAR) 5.4.1 Benzothiadiazole (BTH) Induces SA-Dependent SAR 5.4.1.1

BTH Acts as SAR Inducer in Wide Range of Crop Plants

BTH (benzo[1,2,3]thiadiazole-7-carbothioic acid S-methyl ester) is the most successfully developed commercial compound to activate plant innate immune system and induce SAR. It is the first synthetic chemical developed and marketed as a SAR inducer and is marketed in Europe as BION and as ACTIGARD in USA. (Walters et al. 2005, Vidhyasekaran 2004). BTH activates SAR in many crops against a broad spectrum of diseases caused by oomyctes, fungi, bacteria, and viruses. BTH activates the plant innate immune system in several cereal crop plants including rice (Schaffrath et al. 1997), wheat (Gorlach et al. 1996; Stadnik and Buchenauer 2000; Ge et al. 2001), barley (Besser et al. 2000), and maize (Morris et al. 1998). BTH has been shown to induce defense mechanisms in several horticultural crops including apple (Thomson et al. 1999a, b), pear (Sobiczewski et al. 2001), strawberry (Terry and Joyce 2000), mango (Boshoff et al. 1998), citrus (Agostini et al. 2003), cashew (Lopez and Lucas 2002), potato (Bokshi et al. 2003), tomato (Abbasi et al. 2001), bean (Bigirimana and Höfte 2002), cucumber (Benhamou and Belanger 1998), watermelon (Hopkins 2002), cantaloupe (Smith-Becker et al. 2003), muskmelon (Wang et al. 2008), broccoli (Pajot and Silue 2005), cauliflower (Ziadi et al. 2001), beet (Mouhanna 2000), spinach (Leskovar and Kolenda 2002), lettuce (Bertona et al. 2000), pepper (Buonaurio et al. 2002), chillies (Matheron and Porchas 2002), and rose (Suo and Leung 2002). It also induces resistance in cotton (Colson-Hanks and Deverall 2000), sugarcane (Ramesh Sundar et al. 2001), oilseed rape (Jensen et al. 1998), sunflower (Tosi and Zazzerini 2000; Prats et al. 2002), tobacco (Friedrich et al. 1996), cyclamen (Elmer 2006), and Arabidopsis (Fitzgerald et al. 2004). In monocots, activated resistance by BTH typically is very long lasting, while the lasting effect is less pronounced in dicots (Oostendorp et al. 2001).

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BTH Induces Systemic Acquired Resistance

Systemic Acquired Resistance (SAR) is an induced immune mechanism in plants (Fu and Dong 2013; Vidhyasekaran 2015). SAR is a heightened state of defense against a broad spectrum of pathogens activated throughout a plant following a local infection (Liu et al. 2011a, b). Salicylic acid (SA) accumulation is required for activation of local defenses at the initial site of attack, and in the distant pathogen-free organs for the induction of SAR (Jung et al. 2009; Návarová et al. 2012; Shah and Zeier 2013). SA signaling has been shown to be required for the manifestation of SAR (Wildermuth et al. 2001; Nandi et al. 2004; Jung et al. 2009; Chaturvedi et al. 2012; Du et al. 2012). Transgenic plants expressing the SA degrading enzyme salicylate hydroxylase encoded by the Pseudomonas putida nahG gene have been shown to be deficient in expressing SAR (Vernooij et al. 1994; Lawton et al. 1995). Isochorismate synthase activity is required for SA synthesis (Gaille et al. 2002, 2003; Garcion et al. 2008). The Arabidopsis ics1 mutant, which is deficient in isochorismate synthase 1 activity, has been found to be SAR deficient (Wildermuth et al. 2001; Jung et al. 2009; Chaturvedi et al. 2012). These results suggest that SA signaling system is important in inducing SAR.

5.4.1.3

BTH Elevates NPR1 Gene Transcription to Trigger SAR

NPR1 (NONEXPRESSER OF PR GENES1), the transcription cofactor, is involved in triggering SAR (Durrant and Dong 2004; Fitzgerald et al. 2004; Maier et al. 2011; Hermann et al. 2013; Vidhyasekaran 2015). The npr1 mutant of Arabidopsis thaliana has been shown to be deficient in SAR (Durrant and Dong 2004) and it suggests the importance of NPR1 in the SAR signaling pathway. When SAR is triggered and SA levels increase, the cytosolic redox environment may be altered, resulting in the reduction of intermolecular sulfide bonds that normally keep NPR1 present in the cytosol in an oligomeric form. Once these bonds are reduced, NPR1 is found in a predominantly monomeric form that can translocate into the nucleus (Mou et al. 2003). When NPR1 is localized to the nucleus, it interacts with the TGA family of basic-leucine zipper (bZIP) transcription factors (Kinkema et al. 2000; Fan and Dong 2002). NPR1 enhances the binding of TGA factors to the promoter of PR genes (Johnson et al. 2008). NPR1 is involved in induction of SAR. NPR1 plays important role in inducing high levels of chromatin modification on promoters of the transcription factor genes (Jaskiewicz et al. 2011). Increased activation of NPR1 may result in activation of defense genes and induction of resistance against pathogens (Cao et al. 1997; Chern et al. 2001; Friedrich et al. 2001; Fitzgerald et al. 2004). BTH treatment induces NPR1 mRNA accumulation by several-fold (Chern et al. 2001). Transcript levels of OsNPR1 were elevated by BTH in rice (Yuan et al. 2007). Increased NPR1 gene expression has been correlated with elevated and quicker PR gene expression (Chern et al. 2001; Yuan et al. 2007; Vidhyasekaran 2015).

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Manipulation of SA Carboxyl Methyltransferase (SAMT) and Methyl Salicylate Esterase (MSE) to Trigger SAR Using BTH

SAR is activated throughout a plant following local infection or local treatment (Liu et al. 2011a, b; Shah and Zeier 2013). Induction of SAR may require some mobile signal(s) produced at the site of infection (treatment) to carry the SAR message throughout the plant (Park et al. 2009; Manosalva et al. 2010; Chanda et al. 2011; Návarová et al. 2012; Vidhyasekaran 2015). It has been suggested that methyl salicylate (MeSA) may be a mobile signal involved in the SAR system (Manosalva et al. 2010). MeSA is synthesized from salicylate (SA) via a reaction catalyzed by Sadenosyl-L-methionine (SAM): salicylic acid carboxyl methyl transferase (SAMT) (Xu et al. 2006; Koo et al. 2007; Kwon et al. 2009). SAR development appears to require SAMT in the primary infected tissue to produce MeSA (Park et al. 2007; Liu et al. 2010). OsBISAMT1 (Oryza sativa L. benzothiadiazole [BTH]-induced SAMT1), a gene encoding S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase (SAMT) in rice has been isolated (Xu et al. 2006). BTH treatment induced expression of OsBISAMT1 in rice leaves (Fig. 5.11; Xu et al. 2006). BTH is known to induce disease resistance in rice (Schweizer et al. 1999; Ge et al. 2001; Ahn et al. 2005). Altering expression of SAMT1 has been shown to compromise SAR in Arabidopsis Salicylic acid

BTH Activates

S-adenosyl-L methionine:salicylic acid carboxyl methyl transferase (SAMT)

Methyl salicylate (MESA)

BTH

Methyl salicylate esterase

Systemic movement of MESA

Activates

SA in distal leaves

Induction of SAR Fig. 5.11 BTH triggers SAR development by enhancing the activities of SAMT and MESA-esterase (Adapted from Forouhar et al. 2005; Xu et al. 2006; Park et al. 2007; Kwon et al. 2007)

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(Liu et al. 2010). The results suggest that SAMT1 is required to trigger BTH induced SAR. MeSA is biologically inactive in induction of defense response (Kumar and Klessig 2008; Park et al. 2009). By contrast, SA is a highly active signal inducing expression of defense genes, but SA is transported upward only in small amounts via xylem (Rocher et al. 2006). It seems that MeSA which moves systemically through phloem may be converted to active SA form in the distal systemic tissue (Park et al. 2007, 2009). A high affinity SA-binding protein (SABP) termed SABP2 has been identified in various plants (Kumar et al. 2006; Vlot et al. 2008b; Manosalva et al. 2010; Tripathi et al. 2010; Vidhyasekaran 2015). SABP2 is a methyl salicylate esterase whose function is to convert biologically inactive methyl salicylate to active SA (Kumar and Klessig 2008; Vlot et al. 2008b; Manosalva et al. 2010; Vidhyasekaran 2015). SABP2’s esterase activity is inhibited in the initially primary infected tissue by SA binding in its active site. It results in accumulation of methyl salicylate in the primary infection site, which is then translocated through the phloem to systemic tissue. In the distant systemic tissue methyl salicylate is converted to SA by methyl salicylate esterase (Kumar and Klessig 2008; Park et al. 2009). These results suggest that MeSA biosynthesis by the action of SAMT is required in the primary infected leaves where the SAR signal is produced. In contrast, MeSA esterase (MSE) activity is needed in the uninoculated systemic leaves, where the SAR signal is perceived and processed (Park et al. 2007). MeSA does not induce defense responses (Seskar et al. 1998) and it must be converted to SA by a MSE for biological activity. The SABP2’s MSE activity must be inhibited in the primary infected tissue (by SA binding in its active site pocket) to facilitate the accumulation of sufficient levels of MeSA to signal SAR (Park et al. 2007, 2009). These studies suggest that MeSA is a mobile signal in the SAR development process. BTH may also contribute to the establishment of SAR through an interaction with methyl salicylate esterase that is critical for the perception of defense-inducing signals in systemic tissues (Fig. 5.11; Du and Klessig 1997; Forouhar et al. 2005; Park et al. 2007; Tripathi et al. 2010). Tobacco SABP2 catalyzes the conversion of methyl salicylic acid into salicylic acid to induce SAR (Tripathi et al. 2010). Transgenic SABP2-silenced tobacco plants failed to express SAR when treated with BTH (Tripathi et al. 2010). The results suggest that functional SABP2 is required for BTH-mediated induction of SAR.

5.4.1.5

BTH Induces Priming

Treatment of plants with BTH, which triggers SA signaling, causes the induction of a unique physiological state called “priming” (Conrath 2011; Camañes et al. 2012; Slaughter et al. 2012) When a treatment puts a plant in a state of increased alertness with no or only minimal gene induction it is called priming (Conrath et al. 2002, 2006, 2015; Vidhyasekaran 2015). After localized foliar infections by diverse pathogens or by treatment with synthetic compounds, plants develop whole-plant immunity, called

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SAR (Conrath et al. 2006; Beckers and Conrath 2007; Conrath 2009; Mukherjee et al. 2010). In this process, distal (systemic) leaves become primed to activate stronger defense response upon secondary infection (Beckers et al. 2009; Slaughter et al. 2012). SAR is associated with priming of defense mechanisms (Jung et al. 2009; Luna et al. 2012) and the priming results in a faster and stronger induction of defense mechanisms after pathogen attack (Conrath 2011). BTH is known to induce priming and confer resistance against viral (Mandal et al. 2008), bacterial (Flors et al. 2008), oomycete (Hamiduzzaman et al. 2005; Ziadi et al. 2008) and fungal (Hukkanen et al. 2007; Umemura et al. 2009) diseases.

5.4.1.6

BTH Induced Histone Modifications May Be Involved in Gene Priming in SA-Induced SAR

Nucleus of a cell is made up of chromatin, which is a combination of DNA and proteins (Ouyang and Gill 2009). The primary function of chromatin is to package DNA into a smaller volume to fit in the cell. The first level of compaction is achieved by nucleosomal packaging of DNA. Each nucleosome comprises 147 bp of DNA wrapped around a histone octamer that consists of two molecules each of histone proteins H2A, H2B, H3, and H4 (Probst et al. 2004; Shi and Fang 2011). The primary protein components of chromatin are histones that compact the DNA (Bender 2004). Chromatin, the complex of genomic DNA with specialized proteins is a carrier of heritable information (Pecinka and Scheid 2012). Chromatin structure is important for the regulation of gene expression (Jaskiewicz et al. 2011; Pecinka and Scheid 2012). Chromatin modification acts as a memory for SAR (Jaskiewicz et al. 2011). The histone proteins are subject to various covalent modifications including acetylation, methylation, phosphorylation, and ADP-ribosylation (Britton et al. 2011; Chen et al. 2011). Acetylation of lysines in the amino-terminal tails of histones H3 and H4 has been associated with active genes (Eberharter and Becker 2002). Lysine acetylation is an important modification involved in the regulation of gene expression (Arif et al. 2010). In histone methylation, lysine and arginine residues are methylated and up to three methyl groups are added to each residue. Specific methylation patterns are associated with gene activation and repression. The strongest correlation between histone methylation and gene activity has been reported for trimethylation of Lys4 on histone H3 (H3K4me3) on promoters and coding sequences of active genes (Ruthernburg et al. 2007). Jaskiewicz et al. (2011) showed that histone modifications are systemically set during a priming event. These modifications might create a memory of the primary infection that is associated with an amplified reaction to a second stress conditions. It is known that chromatin states could control cellular memory (Zhang 2008). The primed genes may be poised for enhanced activation of gene expression by histone modification (Jaskiewicz et al. 2011). In the SAR response, defense genes in the infected and distant tissue show the ‘priming’ phenomenon; they are able to respond faster and/or to a greater extent to a subsequent challenge (Kohler et al. 2002; Conrath 2009, 2015; Vidhyasekaran

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2015). The promoters of many of these genes contain at least one ‘W-box’ that provides binding sites for WRKY transcription factors (Rushton et al. 2010). BTH treatment induced a typical priming effect on WRKY 29, WRKY6, and WRKY53 genes (Jaskiewicz et al. 2011). The expression of the WRKY genes was enhanced in BTHtreated plants when the plants were stressed. Water infiltration, a stress inducing cell death after BTH treatment resulted in strongly enhanced gene activation, compared with plants that were stressed without previous BTH treatment. On the WRKY29 promoter, trimethylation (H3K4me3) and dimethylation (H3K4me2) of H3K4 and all acetylations tested increased after BTH application although this did not induce WRKY29 transcription. Thus, chromatin marks normally associated with active genes are set by the priming stimulus before gene activation. After previous priming, a stress stimulus enhanced some of the modifications—H3K4me2, H3K9ac and H4K12ac— on WRKY 29 (Jaskiewicz et al. 2011). Collectively, these results suggest that prestress application of BTH induced chromatin modifications on WRKY gene promoters that facilitate the activation of gene expression by subsequent stress. NPR1 has been shown to be involved in chromatin modification-induced priming (Vidhyasekaran 2015). The npr1 mutant of Arabidopsis thaliana has been shown to be deficient in SAR and this mutant could not be primed for enhanced gene expression (Kohler et al. 2002; Beckers et al. 2009). BTH induced trimethylation of H3K4 on the WRKY29 promoter in the wild-type A. thaliana plants, but not on the primingdeficient npr1 mutant. Similar results were obtained on the studies on WRKY6 and WRKY53 expression and histone modification. Neither gene augmented expression after BTH treatment and stress stimulus in the npr1 mutant. This correlated with the impaired ability of npr1 to induce high H3K4me3 levels on the WRKY6 and WRKY53 promoters in response to BTH (Jaskiewicz et al. 2011). The results suggest that NPR1 plays important role in inducing high levels of chromatin modification on promoters of WRKY genes.

5.4.1.7

BTH Activates MPK3 Gene Expression and Induces Priming and SAR

Mitogen-activated protein kinase (MAPK) cascades are major pathways downstream of receptors that transduce extracellular stimuli into intracellular responses in plants (Hettenhausen et al. 2012; Zhang et al. 2012; Vidhyasekaran 2014). The MAPKs transduce extracellular stimuli into intracellular transcription factors through activation of Ca2+ , ROS, SA, JA, and ethylene-dependent signaling systems, and enhance expression of defense-related genes in plant innate immune system (Vidhyasekaran 2014). Some dormant MAPKs have been suggested to be important components required for priming in Arabidopsis and the prestress deposition of these inactive kinases may be a possible mechanism of priming during development of SAR (Beckers et al. 2009). MPK3, and functionally redundant MPK6, have been found to be important components for full priming in Arabidopsis. BTH activated MPK3 gene expression and induced priming and SAR. Similarly another MAPK gene, MPK6 was

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also found to be involved in priming process. However, the BTH-induced accumulation of MPK6 transcript and protein was less pronounced. Both MPK3 and MPK6 accumulate in an inactive form during priming of Arabidopsis with BTH (Beckers et al. 2009). Both MPK3 and MPK6 displayed greater activity in Arabidopsis plants which are primed and subsequently challenged with the virulent P. syringae pv. maculicola. These two enzymes were more strongly activated in primed plants than in nonprimed plants. Priming of defense gene expression and induced resistance were lost or reduced in mpk3 or mpk6 mutants (Beckers et al. 2009). These results suggest that BTH-induced activation of MPK3 and MPK6 is a critical step in priming plants for full induction of defense responses during induced resistance.

5.4.1.8

Management of Crop Diseases Using BTH

BTH (benzo[1,2,3]thiadiazole-7-carbothioic acid S-methyl ester) is the most successfully developed commercial compound to activate plant innate immune system and induce SAR. It is the first synthetic chemical developed and marketed as a SAR inducer and is marketed in Europe as BION and as ACTIGARD in USA (Walters et al. 2005). BTH activates SAR in many crops against a broad spectrum of diseases caused by oomyctes, fungi, bacteria, and viruses. BTH activates the plant innate immune system in several cereal crop plants including rice (Schaffrath et al. 1997); wheat (Gorlach et al. 1996; Stadnik and Buchenauer 2000; Ge et al. 2001), barley (Besser et al. 2000), and maize (Morris et al. 1998). BTH has been shown to induce defense mechanisms in several horticultural crops including apple (Thomson et al. 1999a, b), pear (Sobiczewski et al. 2001), strawberry (Terry and Joyce 2000), mango (Boshoff et al. 1998), citrus (Agostini et al. 2003), cashew (Lopez and Lucas 2002), potato (Bokshi et al. 2003), tomato (Abbasi et al. 2001), bean (Bigirimana and Höfte 2002), cucumber (Benhamou and Belanger 1998), watermelon (Hopkins 2002), cantaloupe (Smith-Becker et al. 2003), muskmelon (Wang et al. 2008), broccoli (Pajot and Silue 2005), cauliflower (Ziadi et al. 2001), beet (Mouhanna 2000), spinach (Leskovar and Kolenda 2002), lettuce (Bertona et al. 2000), pepper (Buonaurio et al. 2002), chillies (Matheron and Porchas 2002), and rose (Suo and Leung 2002). It also induces resistance in cotton (Colson-Hanks and Deverall 2000), sugarcane (Ramesh Sundar et al. 2001), oilseed rape (Jensen et al. 1998), sunflower (Tosi and Zazzerini 2000; Prats et al. 2002), tobacco (Friedrich et al. 1996), cyclamen (Elmer 2006), and Arabidopsis (Fitzgerald et al. 2004). In monocots, activated resistance by BTH typically is very long lasting, while the lasting effect is less pronounced in dicots (Oostendorp et al. 2001). The efficacy of BTH in management of various crop diseases has been described in Chap. 3.

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3-Chloro-1-Methyl-1H-Pyrazole-5-Carboxylic Acid (CMPA) Activates NPR1 in SA Signaling Pathway

3-chloro-1-methyl-1H-pyrazole-5-carboxylic acid (CMPA) is a SA signaling systemactivating chemical. It acts independently of SA accumulation and requires NPR1 for its function. CMPA acts downstream of SA accumulation and acts in the SA signaling pathway between SA production and NPR1 activity (Yasuda 2007). It protects rice from infection by rice blast pathogen Magnaporthe oryzae and bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Nakashita et al. 2003; Nishioka et al. 2005). It enhances resistance of tobacco to Pseudomonas syringae pv. tabaci and Oidium sp. (Yasuda et al. 2003b).

5.4.2 N-Cyanomethyl-2-Chloroisonicotinamide (NCI) Activates NPR1-Dependent Defense Responses N-cyanomethyl-2-chloroisonicotinamide (NCI) is a potential compound which induces SAR in different plants (Nakashita et al. 2002a). Arabidopsis plants treated with NCI exhibited increased expression of PR-1, PR-2, and PR-5 genes and enhanced resistance to the bacterial pathogen Pseudomonas syringae pv. tomato (Yasuda et al. 2003a). NCI induced the same responses as SA and required a functional NPR1 gene for activation of SAR (Yasuda et al. 2003a). It suggests that NCI activates the SA-mediated defense pathway. However NCI induced disease resistance and PR gene expression in NahG transgenic plants in which SA is degraded, suggesting that NCI does not require SA to induce SAR. In contrast, NCI could not induce the SAR marker PR genes and SAR in the npr1 mutant (Yasuda et al. 2003a). The results suggest that NCI activates SAR by stimulating the site between SA and NPR1 (Yasuda et al. 2003a; Yasuda 2007). NCI has been found to be effective in inducing resistance against Tobacco mosaic virus (TMV), P. syringae pv. tabaci, and Oidium lycopersici in tobacco (Nakashita et al. 2002a; Yasuda 2007). NCI also induces resistance against Magnaporthe oryzae in rice (Nakashita et al. 2002a; Yasuda 2007).

5.4.3 Tiadinil (TDL) Activates NPR1 Gene to Induce SAR Tiadinil (TDL, 3,4-dichloro-N-(2-cyanophenyl)-1,2-thiazole-5-carboxamide) is another potential chemical, which triggers SA signaling pathway by activating NPR1 gene expression (Yasuda et al. 2006). TDL induces SAR independent of SA biosynthesis and it requires a functional NPR1 gene to induce SAR in Arabidopsis (Yasuda 2007). TDL induces resistance against fungal (Oidium lycopersici), bacterial (Pseudomonas syringae pv. tabaci) and viral (Tobacco mosaic virus) pathogens of tobacco

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(Nakashita et al. 2002a; Yasuda et al. 2004; Tsubata et al. 2006; Yasuda 2007). TDL has been developed as a commercial product by Nihon Nohyaku Co., and is practically used to control rice blast disease (Yasuda et al. 2006).

5.4.4 SV-03 Activates NPR1 Gene to Induce SAR SV-03 is a metabolite of 3,4-dichloro-N-(2-cyanophenyl)-1,2-thiazole-5carboxamide (Tiadinil, TDL). It stimulates SA signaling pathway downstream of SA production (Yasuda et al. 2006). When NahG transgenic tobacco plants unable to accumulate SA due to the expression of the SA degrading bacterial enzyme salicylate hydroxylase were treated with SV-03, the plants showed increased resistance against TMV and P. syringae pv. tabaci similar to the wild-type plants treated with SV-03. SV-03 induced the expression SAR-related PR-1, PR-2, and PR-5 genes in both NahG transgenic and wild-type plants (Yasuda et al. 2006). The results suggest that SV-03 does not require SA to induce SAR-like disease resistance in tobacco. Studies conducted with Arabidopsis plants revealed that induction of SAR by SV-03 was independent of SA biosynthesis but required a functional NPR1 gene to induce SAR in Arabidopsis (Yasuda 2007). SV-03 triggers resistance against various viral, bacterial and fungal pathogens in tobacco (Nakashita et al. 2002a; Yasuda 2007).

5.5 Molecular Manipulation of SA Signaling System by Probenazole for Crop Disease Management Probenazole (3-allyloxy-1,2-benzisothiazole-1,1-dioxide) and its metabolite 1,2benzisothiazole-3 (2H)-one 1,1-dioxide (BIT, saccharin) are potential plant defense activators and both of them are known to induce SA accumulation and activate SA signaling system (Schreiber and Desveaux 2008). Probenazole induces phenylalanine ammonia-lyase (PAL) gene activation and PAL is known to be involved in SA biosynthesis (Fig. 5.13; Lin et al. 2008). Probenazole treatment induces a gene (OsSGT1) encoding UDP-glucose: SA glucosyl transferase (SGT) (Fig. 5.12; Umemura et al. 2009). The enzyme catalyses the conversion of free SA to SA-Obeta-glucoside (SAG) (Song 2006; Vidhyasekaran 2015). Excess amount of free SA is phytotoxic and SGT regulates the free SA levels by forming SAG (Shapiro and Gutsche 2003). SAG is less phytotoxic and inactive in inducing defense responses. SAG is converted back to free SA by endogenous hydrolases (Shulaev et al. 1997) and the free SA induces SAR (systemic acquired resistance)-related genes (Umemura et al. 2009). SAG accumulated in rice leaf tissue following treatment with probenazole. RNAi-mediated silencing of the OsSGT1 gene significantly reduced the

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Phenylalanine

Probenazole activation

Phenylalanine ammonia-lyase

trans-cinnamic acid

Probenazole

Benzoic acid

Salicylic acid

activates

S-adenosyl L-methionine salicylic acid carboxyl methyltransferase

UDP-SA glucosyl transferase (SAGT)

SA-O –βglucoside(SAG)

SA-βglucosidase activates

Methyl salicylate Methyl salicylate esterase

Salicylic acid

Probenazole

Salicylic acid

Activation

NPR1

Induction of SAR

Fig. 5.12 Induction of SA signaling system by probenazole (Adapted from Yoshioka et al. 2001; Lin et al. 2008; Umemura et al. 2009)

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probenazole-dependent development of resistance against the blast pathogen Magnaporthe oryzae (Umemura et al. 2009). These results suggest that OsSGT1 gene mediates the probenazole-induced defense signaling system and confers disease resistance. BIT treatment did not induce any significant increase in free SA level in Arabidopsis plants. However, the level of total SA (free SA + SAG) content in BIT-treated plants was approximately twofold greater than that detected in the control plants (Yoshioka et al. 2001). It suggests that BIT induces accumulation of SAG rather than free SA in treated Arabidopsis plants. The results observed in Arabidopsis plants were similar to that observed in probenazole-treated rice plants (Umemura et al. 2009). BIT has been shown to induce the expression of S-adenosyl-L-methionine (SAM): salicylic acid carboxyl methyl transferase (SAMT) in Atropa belladonna. The enzyme is responsible for the conversion of SA to methyl salicylate (MeSA) (Kwon et al. 2009). MeSA is inactive in inducing defense response; however, MeSA may be involved in systemic movement of SA in plants. It has been suggested that MeSA moves systemically through phloem to distal tissues, where it is converted back to the active SA form (Park et al. 2007, 2009). The results suggest that BIT activates the SA signaling system both at SA accumulating stage and at MeSA biosynthesis stage in A. belladonna. BIT treatment induces SAR marker gene PR-1 in Arabidopsis. No PR-1 expression was detected in BIT-treated plants containing npr1 mutation. Plants containing the npr1mutation failed to develop resistance to Peronospora parasitica or Pseudomonas syringae pv. tomato (Yoshioka et al. 2001). The results suggest that probenazole/BIT intervenes in SA signaling system at SA accumulation stage as well as at NPR1 stage to trigger resistance against pathogens (Fig. 5.12). Probenazole induces several defense genes. A probenazole-responsive gene, RPR1, has been cloned (Sakamoto et al. 1999). RPR1 contains a nucleotide binding site and leucine-rich repeats, thus sharing structural similarity with known disease resistance (R) genes. RPR1 was induced during the systemic induced resistance (Sakamoto et al. 1999). Probenazole induced expression of several pathogenesisrelated genes and accumulation of salicylic acid in A. thaliana (Yoshioka et al. 2001). Probenazole induced expression of PR-1, PR-2, and PR-5 genes in Arabidopsis (Lawton et al. 1996). Tobacco plants treated with probenazole or BIT exhibited increased expression of several pathogenesis-related (PR) genes and increased levels of free and total SA (Midoh and Iwata 1996; Nakashita et al. 2002b). Probenazole treatment enhances the activation of various defense-related enzymes, such as peroxidase, lipoxygenase, PAL, and ACC synthase in rice inoculated with Magnaporthe oryzae (Iwata et al. 1980; Sekizawa et al. 1987). Probenazole may function as a SAR activator or as a priming effector that enhances defense responses following pathogen infection. Proteomic analysis of rice defense response induced by probenazole revealed that phenylalanine ammonia-lyase (PAL), caffeic acid 3O-methyltransferase (COMT), and glutathione S-transferase (GST) are induced by probenazole. These enzymes are likely to confer probenazole-induced resistance in rice via such functions as biosynthesis and transport of flavonoid-type phytoalexin and/or lignin biogenesis (Lin et al. 2008).

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Probenazole or BIT treatment did not induce disease resistance and PR-1 expression in NahG transgenic plants which are unable to accumulate SA due to expression of the SA-degrading enzyme salicylate hydroxylase. The results suggest that probenazole and BIT induce SAR by triggering signaling at a point upstream of SA function (Nakashita et al. 2002b). Probenazole appears to be potential tool for management of fungal and bacterial pathogens in rice. Probenazole has been developed as a commercial product and marketed as Oryzemate (Oostendorp et al. 2001; Iwai et al. 2007). Probenazole effectively controls rice blast (Magnaporthe oryzae) and bacterial blight (Xanthomonas oryzae pv. oryzae) by inducing various defense genes (Oostendorp et al. 2001). Probenazole treatment could induce SA accumulation only in adult rice plants, not in young plants. The chemical did not influence the development of blast lesions in the susceptible interaction and there was no accumulation of SA and PR proteins in young leaves (Iwai et al. 2007). These studies suggest that probenazole-induced resistance in rice is age-dependently regulated via SA accumulation. Probenazole induces resistance against the bacterial pathogen Pseudomonas syringae pv. tomato and the oomycete pathogen Peronospora parasitica in Arabidopsis (Yoshioka et al. 2001). Probenazole induces enhanced resistance to the viral pathogen Tobacco mosaic virus, the bacterial pathogen Pseudomonas syringae pv. tabaci, and the fungal pathogen Oidium sp. in tobacco (Nakashita et al. 2002b).

5.6 Induction of Transgenerational SAR by BABA The nonprotein amino acid β-aminobutyric acid (BABA) induces broad-spectrum resistance in a range of crops (Cohen 2002). BABA potentiates mRNA accumulation of the SA-associated PR-1, but not the JA/ET dependent PDF1.2 gene and it induces protection against the necrotrophic fungus Botrytis cinerea in Arabidopsis (Zimmerli et al. 2001). The results suggest that BABA induces resistance against B. cinerea through activation of SA-dependent signaling system in Arabidopsis. BABA induces resistance against the bacterial pathogen Pseudomonas syringae pv. tomato by activating SA signaling pathway (Zimmerli et al. 2000). BABA treatment strongly decreased disease symptoms caused by P. syringae pv. tomato in Arabidopsis (Zimmerli et al. 2000). BABA treatment conditioned the plant to produce PR-1 mRNA more rapidly. PR-1 mRNA expression in plants inoculated with the virulent bacterial pathogen Pseudomonas syringae pv. tomato was induced 12 h earlier in BABA-treated plants compared with the untreated control in A. thaliana plants (Zimmerli et al. 2000). It could not induce resistance against P. syringae pv. tomato in NahG-expressing Arabidopsis plants and also in npr1 mutant Arabidopsis plants. In contrast, mutants deficient in JA or ethylene signaling pathways were protected against the bacterial pathogen at a similar level as the wild-type plants (Zimmerli et al. 2000). These results suggest that BABA induces resistance against the bacterial pathogen by triggring SA pathway.

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SA (ng g-1 400 freshwt) 300 200 100 0 Control

BABA

Fig. 5.13 Accumulation of SA in tobacco plants treated with BABA (Adapted from Siegrist et al. 2000)

BABA induces resistance against Tobacco mosaic virus (TMV) in tobacco. BABA-mediated enhancement of resistance in tobacco to TMV was found to be strictly dependent on SA-mediated signal transduction since it could not be detected in salicylate hydroxylase expressing transgenic tobacco plants. BABA treatment induced local and systemic increase of SA levels (Fig. 5.13; Siegrist et al. 2000). It also induced the expression of PR-1, a molecular marker of SAR in tobacco (Siegrist et al. 2000). The results suggest that BABA- induced SAR is dependent on the accumulation of SA (Siegrist et al. 2000). BABA induces priming in the SAR induction pathway. The induced priming in Arabidopsis thaliana has been found to be inherited epigenetically from diseaseexposed plants. The descendants of primed plants exhibited next-generation systemic acquired resistance (Luna et al. 2012; Slaughter et al. 2012). The descendants of A. thaliana plants that had been primed with BABA showed a faster and higher accumulation of transcripts of defense-related genes in SA signaling pathway and enhanced disease resistance upon challenge inoculation with the bacterial pathogen Pseudomonas syringae (Slaughter et al. 2012). The progeny of the primed plants was also more resistant against the oomycete pathogen Hyaloperonospora arabidopsidis. When transgenerationally primed plants were subjected to an additional priming treatment, their descendants displayed an even stronger primed phenotype (Slaughter et al. 2012). The results suggest that plants can inherit a sensitization for the priming phenomenon and the primed state of plants is transferred to their progeny. The transgenerational SAR was found to be sustained over one stress-free generation, indicating an epigenetic basis of the phenomenon (Luna et al. 2012). SA-inducible promoters of the transcription factors WRKY6 and WRKY53 in the progeny from plants showing transgenerational SAR were found to be enriched with acetylated histone H3 at lysine 9, a chromatin mark associated with a permissive state of transcription (Luna et al. 2012). The results suggest the importance of chromatin remodeling in the transgenerational SAR (Luna et al. 2012).

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5.7 Manipulation of SA Signaling System Using Plant-Derived Products for Disease Management 5.7.1 Azelaic Acid Azelaic acid is a signal molecule triggering plant defense responses and it acts almost similar to oligogalacturonide as a host-associated molecular pattern (HAMP). It is a dicarboxylic acid compound. It is a natural compound found in Arabidosis, wheat, rye, barley and many other plants. When the plants are attacked by pathogens, the plant greatly increases the production of azelaic acid, which is then transported via the plant’s vascular system to other parts of the plant. Azelaic acid does not directly induce defense responses, but confers on the plants the ability to mount a faster and stronger defense response if and when the plant is attacked again (Jung et al. 2009). It does this by increasing the production of SA. Azelaic acid stimulates the production of AZ11, a protein which helps prime the plant to build up its immunity by generating additional SA (Jung et al. 2009). Azelaic acid is a pathogen-induced metabolite in vascular sap that has several properties of a long-distance resistance-priming signal (Parker 2009). Azelaic acid may strengthen the induction of systemic immunity in plants (Návarová et al. 2012; Zoeller et al. 2012; Shah and Zeier 2013). When pure azelaic acid was sprayed onto leaves, it induced systemic resistance against the bacterial pathogen Pseudomonas syringae in Arabidopsis (Zahn 2009). Since azelaic acid only primes a plant’s immune system, its use may not create a burden on the plant or otherwise detract from plant’s health or productivity. Azelaic acid is a natural compound found in several plants. It is safe and has been widely tested in humans. It is used in enhancing human immune response. It is commercially available as anti-microbial creams to treat acne and rosacea in humans. Azelaic acid has been patented and commercial product is likely to be available soon. Overexpression of AZI1 in Arabidopsis induced disease resistance (www.faqs.org/patents/ app/20090048312).

5.7.2 AHO, a Product from Strobilanthes Strobilanthes cusia, a perennial plant cultivated in several Asian countries and also found in hilly regions as wild plant. It is a medicinal plant and the plant is also used for preparation of a dye. A derivative of isatin, 3-acetonyl-3-hydroxyoxindole (AHO), isolated from the extracts of S. cusia has been identified as a potential activator of SA signaling system (Li et al. 2008). When tobacco plants were treated with AHO, SA accumulated in the leaf tissues accompanied by increased levels of PR-1 gene expression, and phenylalanine ammonia-lyase (PAL) activity. AHO induced enhanced resistance to Tobacco mosaic virus and to the powdery mildew pathogen Blumeria cichoracearum (Li et al. 2008). AHO treatment did not induce TMV resistance or PR-1 expression in nahG transgenic plants expressing salicylate

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hydroxylase, which prevents the accumulation of SA. It suggests that AHO acts upstream of SA signaling pathway (Li et al. 2008). It appears that AHO is a potential elicitor of defense responses and can be used as a tool to manage crop diseases.

5.7.3 Burdock Plant Oligosaccharide Product An oligosaccharide product obtained from burdock (Arctium lappa) plant induced the production of volatile compounds involved in defense signaling system in tomato. The burdock oligosaccharide induced methyl salicylate in tomato plants (He et al. 2006). Methyl salicylate (MeSA) is synthesized from SA (Kwon et al. 2009). MeSA is a phloem-mobile signal and biologically inactive in induction of defense response. It moves systemically to the noninfected tissues and is associated with induced systemic resistance (Park et al. 2007, 2009; Kumar and Klessig 2008; Vlot et al. 2008a, b; Manosalva et al. 2010). SA is a highly active signal inducing expression of defense genes, but SA is transported upward only in small amounts via xylem (Rocher et al. 2006). A high affinity SA-binding protein (SABP) termed SABP2 has been identified in plants (Forouhar et al. 2005; Kumar et al. 2006; Vlot et al. 2008b). SABP2 is a methyl salicylate esterase whose function is to convert biologically inactive methyl salicylate to active SA (Kumar and Klessig 2008; Vlot et al. 2008b). SABP2’s esterase activity is inhibited in early stages by SA binding in its active site; this facilitates accumulation of methyl salicylate, which is then translocated through the phloem to systemic tissue for perception and processing by SABP2 to SA (Kumar and Klessig 2008; Park et al. 2009). The results suggest suggest that MeSA is a critical mobile signal and on conversion of MeSA to SA, SA and not MeSA activates the expression of defense genes. The burdock oligosaccharide has been found to be effective in inducing SA-induced systemic resistance contolling the gray mold disease caused by Botrytis cinerea in tomato (He et al. 2006).

5.8 N-Acyl-L-Homoserine Lactones (AHLs)–Producing Bacteria Induce SA-Dependent Systemic Resistance N-acyl-L-homoserine lactones (AHLs) are structural analogs of alkamides. Serratia liquefaciens MG1 and Pseudomonas putida IsoF colonize tomato roots, produce AHL in the rhizosphere and increase systemic resistance of tomato plants against Alternaria alternata. The AHL-negative mutant S. liquefaciens MG44 was less effective in reducing disease symptoms as compared to the wild-type bacteria. Salicylic acid levels were increased in leaves when AHL-producing bacteria colonized the rhizosphere (Schuhegger et al. 2006). The results suggest that AHL may be a systemic signal in triggering salicylic acid-mediated defense responses in tomato and these bacteria can be exploited for management of crop diseases.

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5.9 Activation of SA-Dependent Signaling System by Rhizobacteria for Management of Crop Diseases Some of the rhizobacterial strains activate the plant innate immune system by triggering SA signaling system. Treatment of tobacco plants with Bacillus pumilus strain SE34 triggered increased accumulation of salicylic acid compared with that of nontreated plants, 1 day after challenge-inoculation with the blue mold pathogen Peronospora tabacina (Zhang et al. 2002). It induced resistance against the blue mold pathogen in tobacco (Zhang et al. 2002). The induced systemic resistance by P. aeruginosa strain 7NSK27 in tobacco against Tobacco mosaic virus depends on in planta SA accumulation (De Meyer et al. 1999). The P. aeruginosa strain 7NSK27 strain could not induce resistance in transgenic NahG tomato plants in which SA is converted to catechol (Brading et al. 2000), suggesting that the strain activates the plant immune system by activating SA signaling system. Tjamos et al. (2005) reported that the rhizobacterium Paenibacillus alvei K-165 induced defense response against the wilt pathogen Verticillium dahliae in Arabidopsis by activating the SA signaling system involing the components of the pathway from isochorismate and a functional NPR1 (Tjamos et al. 2005).

5.10 Manipulation of SA Signaling System Using Yeast Elicitor for Disease Management SA signaling system can be activated by some MAMPs (for Microbe-associated molecular patterns) for effective crop disease management (Vidhyasekaran 2015, 2016). Treatment of Arabidopsis plants with an autoclaved yeast (bakers yeast; Saccharomyces cerevisiae) suspension induced systemic resistance against bacterial and fungal pathogens (Raacke et al. 2006). The yeast elicitor treatment induced significant changes in expression of several genes in A. thaliana (Raacke et al. 2006). It enhanced expression of the SA-responsive genes encoding PR-1, PR-2, and PR-5. In contrast, expression of genes positively regulated by JA and ethylene was not increased (Raacke et al. 2006). The yeast treatment reduced the bacterial growth and disease symptom development when the bacterial pathogen Pseudomonas syringae was inoculated in the wild-type Arabidopsis plants. However, this treatment did not result in lower bacterial growth or reduced symptoms in the npr1 mutants which are insensitive to SA and also in the NahG-expressing plants which do not accumulate SA. The Arabidopsis mutants opr3, dde2, and jin1 exhibited a similar protective effect of yeast treatment as the wild types. The opr3 and dde2 mutants are defective in JA biosynthesis while jin1 is defective in JA signaling (Raacke et al. 2006). Collectively these results suggest that the yeast elicitor may activate the innate immunity system through SA-dependent signaling system, and JA and ET signaling systems may not be involved in the yeast-induced defense response.

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The yeast elicitor effectively controlled oomycete, fungal, and bacterial pathogens in many crops. It controlled late blight of potato and tomato caused by the oomycete Phytophthora infestans (Tosun 2007). It was effective in reducing infection of the biotrophic fungal pathogens Uncinula necator in grapevine (Tosun 2007) and Blumeria graminis f. sp. hordei in barley (Reglinski et al. 1994a, b). It also induced resistance against necrotrophic fungal pathogen Botrytis cinerea in Arabidopsis (Raacke et al. 2006).

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Chapter 6

Bioengineering and Molecular Manipulation of Jasmonate Signaling System to Activate Plant Immune System for Crop Disease Management

Abstract Jasmonates (JA) are cellular signal molecules regulating the plant innate immunity. The concentrations of JA in healthy unperturbed plant tissues are very low. JA concentration can be increased by enhancing the activities of the enzymes involved in JA biosynthesis. The key enzymes involved in the biosynthesis involve phospholipases, lipoxygenases (LOXs), allene oxide synhases (AOS), allene oxide cyclase (AOC), and OPDA reductase (OPR). The genes encoding these enzymes have been cloned and engineered to enhance the JA biosynthesis and JA accumulation will activate plant immune system. LOX genes have been cloned from different plants. Constitutive overexpression of LOX genes has been shown to be required for conferring resistance against diseases. A 9-lipoxygenase gene, DkLOX3, has been cloned from persimmon plants. The Arabidopsis plants overexpressing the persimmon DkLOX3 gene showed resistance to both bacterial and fungal pathogens. An LOX gene, LOX1, has been cloned from tobacco. The transgenic tobacco plants constitutively expressing LOX1 showed increased resistance against the oomycete pathogen Phytophthora parasitica var nicotianae. A pepper 9-LOX gene, CaLOX1, which encodes a 9lipoxygenase, was isolated from pepper leaves. Overexpression of CaLOX1 in Arabidopsis thaliana conferred enhanced resistance to bacterial, oomycete and fungal pathogens. An allene oxidase synthase gene, OsAOS2 was cloned from rice plants. Transgenic rice plants overexpressing OsAOS2 showed increased resistance against the blast disease. Alkamide treatment enhanced the expression of genes encoding enzymes for jasmonic acid biosynthesis. It enhanced the expression of lipoxygenase genes (LOX2 and LOX3), allene oxide synthase gene (AOS), allene oxide cyclase2 gene (AOC2), and OPDA reductase3 (OPR3) gene. It induces resistance against Botrytis cinerea infection in Arabidopsis. The alkamide-induced resistance depends on activation of JA signaling system. The alkamide treatment induced the expression of the JA-inducible genes JAZ8, VSP2 and ERF2. The alkamide has great potential to combat pathogens by triggering JA biosynthesis pathway. Chitosan triggers lipoxygenase activity and induces accumulation of jasmonic acid. Chitosan activates plant innate immune system and controls several crop diseases. Arachidonic acid isolated from microbes is an elicitor of plant defense responses. Bioengineering technology has been developed to make the plants themselves to produce arachidonic acid without any pathogen invasion. Production of arachidonic acid in a higher plant was achieved using genes encoding enzymes participating in the 3/68 -desaturation © Springer Nature B.V. 2020 P. Vidhyasekaran, Plant Innate Immunity Signals and Signaling Systems, Signaling and Communication in Plants, https://doi.org/10.1007/978-94-024-1940-5_6

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biosynthetic pathways for the formation of C20 polyunsaturated fatty acids. The arachidonic acid-containing transgenic plants showed increased levels of jasmonic acid. The transgenic plants showed enhanced expression of LOX3 gene encoding lipoxygenase and AOS gene encoding allene oxide synthase. The transgenic plants showed increased expression of DGL gene encoding phospholipase A. Developing transgenic plants constitutively producing arachidonic acid may be a potential approach to activate JA pathway for management of plant diseases. Hexanoic acid is a nine carbon dicarboxylic acid that acts as an inducer of plant defenses by means of a priming mechanism. Hexanoic acid induces JA-dependent defense responses by priming. Hexanoic acid has been reported to be a potent natural priming agent of proven efficacy in a wide range of host plants and pathogens. Priming for JAdependent defenses using hexanoic acid appears to be an effective tool for management of crop diseases. Ulvan is a plant defense activator derived from the green algae belonging to the Ulva genus. Ulvan treatment induces elevation of JA content in plants. It induces the expression of well-known jasmonic acid-responsive genes including lipoxygenase, hydroxyproline-rich glycoproteins, proline-rich proteins, defensin and wound-induced protein. Ulvan activates JA-amino acid synthase, which is involved in Jasmonoyl-isoleucine (JA-Ile) biosynthesis. JA-Ile has been shown to be involved in defense signaling. Ulvan effectively controlled several diseases. Several transcription factor genes have been engineered to manipulate JA signaling system for crop disease management. Application of Trichoderma asperellum, Trichoderma virens, T. harzianum, and Pseudomonas putida strains activates JA signaling system and induces systemic resistance. Keywords Bioengineering LOX, AOS, AOC, OPR genes · Chitosan · Arachidonic acid · Hexanoic acid · Priming · Ulvan · Trichoderma—activated JA signaling system · Pseudomonas—activated JA signaling system

6.1 Jasmonate Signaling System Triggers Local and Induced Systemic Resistance Jasmonic acid and their derivatives are important signal molecules detected in a wide spectrum of plant species (Farmer et al. 2003; Balbi and Devoto 2008; Kang et al. 2006; Wasternack 2007; Kazan and Manners 2008; Fonseca et al. 2009; Kombrink 2012; Wasternack and Hause 2013; Vidhyasekaran 2014, 2015, 2016; Gleason et al. 2016; Carvalhais et al. 2017; Liu et al. 2017). The concentrations of JA in healthy unperturbed plant tissues are very low. However, JA accumulates in plants infected by pathogens and/or treated with elicitors (Wang et al. 2000; Fabro et al. 2008; Chehab et al. 2011). Jasmonates are cellular signal molecules with key functions on the regulation of immune responses against pathogens (Pieterse et al. 2012a, b; Thaler et al. 2012; Vidhyasekaran 2015). JA signaling system activates transcription of several defense-genes in plants. It activates transcription of several defense-related PR genes including PR-1, PRB-1b, PR-2 (β-1,3-glucanase), ChiB (PR-3; basic chitinase), PR4 (hevein-like protein), PR-5 (osmotin), PDF1.2 (PR-12; defensin), Thi2.1 (PR-13;

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thionin), and germin-like proteins in Arabidopsis (Zhou et al. 2005; Cao et al. 2006; Johansson et al. 2006; Jung et al. 2007; Lee et al. 2007; Oñate-Sánchez et al. 2007; Pré et al. 2008). JA treatment induced eight defense genes consisting of PR1.1, PR2 (β-1,3-glucanase), PR3 (chitinase), PR4 (wheatwin), PR5 (thaumatin-like protein), TaPERO (peroxidase), PR10, and TaGLP2a (germin-like) in wheat (Ellis and Turner 2001; Jayaraj et al. 2004; Desmond et al. 2006). Activation of JA signaling system induces resistance against necrotrophic fungal pathogens (Thomma et al. 1998; Anderson et al. 2004; Johansson et al. 2006; Zheng et al. 2006; Flors et al. 2008; Korolev et al. 2008; Pré et al. 2008; Gao et al. 2009; Kidd et al. 2009; Vicedo et al. 2009; Wang et al. 2009; Zander et al. 2012; Méndez-Bravo et al. 2011; Moffat et al. 2012; Yan et al. 2012; An and Mou 2013; Vidhyasekaran 2015; Martinez-Medina et al. 2013; Liu et al. 2017; Pathak et al. 2017). It also induces resistance against oomycete (Thomma et al. 2001; Ueeda et al. 2006; Adie et al. 2007) and bacterial (Thomma et al. 2001; Uji et al. 2016) pathogens. JA signaling system is also involved in triggering systemic resistance against pathogens. Two distinctly different types of systemic induced resistance have been recognized. These include “Systemic acquired resistance [SAR]” and “Induced systemic resistance [ISR]”. SAR is a systemic defense network that is usually induced in plants in response to attack by biotrophic and hemibiotrophic pathogens in plants (Liu et al. 2011a, b; Sharon et al. 2011; Po-Wen et al. 2013; Vidhyasekaran 2015). SA signaling has been shown to be required for the manifestation of SAR (Shah 2009; Du et al. 2012; Návarová et al. 2012; Shah and Zeier 2013). ISR is triggered mostly by biocontrol agents (BCAs) and necrotrophic fungi. It is dependent mostly on JA signaling system (Kravchuk et al. 2011; Niu et al. 2011; Weller et al. 2012; Zamioudis and Pieterse 2012; Bakker et al. 2013; Vidhyasekaran 2015).

6.2 Bioengineering Genes Encoding Enzymes in JA Biosynthesis Pathway 6.2.1 Enzymes Involved in JA Biosynthesis Pathway The concentration of jsmonic acid (JA) in healhy plant tissues is very low (Wang et al. 2000). The production of jasmonic acid (JA) in plants is a tightly regulated process (Balbi and Devoto 2008; Kazan and Manners 2008; Wasternack and Hause 2013). JA accumulates in plants treated with elicitors (Wang et al. 2000; Fabro et al. 2008; Chehab et al. 2011). JA signaling systems modulate plant immune responses and confer resistance against different pathogens. (Thomma et al. 1998; Kidd et al. 2009; Vicedo et al. 2009; Méndez-Bravo et al. 2011; Moffat et al. 2012; Vidhyasekaran 2015). JA biosynthesis in stressed plant tissues begins with release of linolenic acid from membranes (Wang et al. 2000). Several enzymes are involved in biosynthesis of JA. The key enzymes involved in the biosynthesis involve phospholipases, lipoxygenases (LOXs), allene oxide synhases (AOS), allene oxide cyclase (AOC), and OPDA

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reductase (OPR) (Vidhyasekaran 2015). Several phospholipase A1 (PLA1) enzymes have been reported to be involved in release of linolenic acid from membrane (Wasternack 2007; Ellinger et al. 2010). The released linolenic acid is oxygenated by LOXs to hydroperoxide derivatives. Further reaction is catalysed by AOS that converts 13-hydroperoxy-linolenic acid (13-HPOT) to an unstable allene oxide intermediate, which is in turn modified by AOC to form 12-oxo-phytodienoic acid (OPDA). Four functional allene oxide cyclase isoforms (AOC1, AOC2, AOC3 and AOC4) have been identified in Arabidopsis thaliana (Stenzel et al. 2012; Otto et al. 2016). OPDA is reduced by OPDA reductase 3 (OPR3) to 3-oxo-2-(2 -pentenyl) cyclopentane-1-octanoic acid (OPC-8:0), which is followed by three rounds of β-oxidation to form 3-ketoacyl-CoA. Three key enzymes, such as acyl-CoA oxidase (ACX), multifunctional protein (MFP) possessing 2-trans enoyl-CoA hydratase and L-3-hydroxyacyl-CoA dehydrogenase activities, and 3-ketoacyl-CoA thiolase (KAT), are responsible for carrying out the fatty acid β-oxidation to form jasmonic acid (JA) (Fig. 6.1; Vidhyasekaran 2007a, b; Wasternack 2007; Balbi and Devoto 2008; Wasternack and Kombrink 2010; Kombrink 2012; Stenzel et al. 2012; Wasternack and Hause 2013; Christensen et al. 2014; Vidhyasekaran 2015; Gleason et al. 2016; Otto et al. 2016; Hou et al. 2018).

6.2.2 Engineering Lipoxygenase Genes to Develop Disease-Resistant Plants Lipoxygenase (LOX) is an important enzyme in the octadecanoid pathway leading to the biosynthesis of jasmonates (Schaller 2001; Zhao et al. 2004). Lipoxygenases are ubiquitous in plants (Brash 1999; Feussner and Wasternack 2002). Plant LOXs are classified as 9-LOXs or 13-LOXs according to the position at which oxygen is incorporated into linoleic acid or linolenic acid, the substrates for LOX catalysis (Brash 1999; Feussner and Wasternack 2002). LOX gene expression and activity are very low in healthy plant tissues and are highly enhanced in response to elicitor treatment (Mene-Saffrané et al. 2003). Constitutive overexpression of LOX gene has been shown to be required for conferring resistance against diseases (Mene-Saffrané et al. 2003). The 9-lipoxygenase ZmLOX12 has been shown to be required to mount an effective jasmonate-mediated defense against Fusarium verticilloides in maize (Christensen et al. 2014). A 9-lipoxygenase gene, DkLOX3, has been cloned from persimmon plants (Hou et al. 2018). The persimmon lipoxygenase gene was used to develop transgenic Arabidopsis plants. The Arabidopsis plants overexpressing the persimmon DkLOX3 gene showed resistance to the bacterial pathogen Pseudomonas syringae pv. tomato and the fungal pathogen Botrytis cinerea (Hou et al. 2018). An LOX gene, LOX1, has been cloned from tobacco (Mene-Saffrané et al. 2003). Tobacco plants were transformed with the LOX1 coding sequence fused to the CaMV 35S promoter. The transgenic plants showed enhanced levels of LOX protein and also enhanced LOX activity

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Releases linolenic acid from cell membrane

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β-oxidation (3X)

Jasmonic acid

Fig. 6.1 Enzymes involved in JA biosynthesis pathway (Adapted from Wasternack and Hause 2013; Vidhyasekaran 2015)

compared to control plants. The transgenic tobacco plants constitutively expressing the inducible lipoxygenase gene LOX1 showed increased resistance against the oomycete pathogen Phytophthora parasitica var nicotianae (Mene-Saffrané et al. 2003). A pepper 9-LOX gene, CaLOX1, which encodes a 9-lipoxygenase, was isolated from pepper leaves (Hwang and Hwang 2010). Overexpression of CaLOX1 in Arabidopsis thaliana conferred enhanced resistance to Pseudomonas syringae pv. tomato, Hyaloperonospora arabidopsidis, and Alternaria brassicicola (Hwang and Hwang 2010).

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6.2.3 Engineering Allene Oxide Synthase Gene to Trigger JA Production for Crop Disease Management Allene oxide synthase (AOS) has been shown to promote JA biosynthesis (Wang et al. 1999). AOS catalyzes the first step in the biosynthesis of jasmonic acid from lipoxygenase-derived hydroperoxides of free fatty acids (Sivasankar et al. 2000). Overexpression of the flax AOS cDNA under the regulation of the cauliflower mosaic virus 35S promoter in transgenic potato plants led to an increase in the endogenous level of JA. Transgenic plants had 6- to 12-fold higher levels of JA than nontransformed plants (Harms et al. 1995). Transgenic tobacco plants containing a flax AOS cDNA under the control of a tetracycline-inducible promoter were generated (Wang et al. 1999). Induction of the flax AOS gene in transgenic plants with chlor-tetracycline led to the expression of the flax AOS mRNA and protein, which resulted in high level of metabolism of 13(S)- hydroperoxyoctadecatrienoic acid (13(S)-HPOT) and formation of 12-oxo-phytodienoic acid (12-O-PDA). Overexpression of the flax AOS alone did not enhance JA levels in healthy, undamaged leaf tissues. However, in wounded tissues overexpressing the flax AOS, levels of JA dramatically increased when compared to those not expressing the flax AOS (Wang et al. 1999). The results suggest that the inducible AOS gene expression triggers JA biosynthesis effectively. A pathogen-inducible allene oxidase synthase gene, OsAOS2 was cloned from rice plants. The basal level of OsAOS2 expression was very low in rice leaves. The expression of OsAOS2 in rice leaves was very much increased upon infection by the rice blast pathogen Magnaporthe grisea (Mei et al. 2006). Transgenic rice plants carrying the OsAOS2 transgene under the control of a strong, pathogen-inducible PBZ1 promoter were developed. These transgenic plants accumulated abundant OsAOS2 transcripts and high levels of JA (Fig. 6.2; Mei et al. 2006). The transgenic plants showed much more accumulation of the AOS transcripts and JA after M. grisea infection. These transgenic rice plants overexpressing OsAOS2 showed increased

Fig. 6.2 Increases in jasmonic acid content in transgenic rice plants overexpressing OsAOS2, the allene oxide synthase gene (Adapted from Mei et al. 2006)

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resistance against the blast disease (Mei et al. 2006). These results suggest that AOS gene is a potential tool for developing disease-resistant plants.

6.3 Manipulation of Genes Encoding Enzymes Involved in JA Biosynthesis Using Alkamide Alkamides are fatty acid amides, which are commonly present in plants (MéndezBravo et al. 2011). N-isobutyl decanamide, the most highly active alkamide, has been shown to be a potential tool to manipulate enzymes involved in JA biosynthesis pathway. The alkamide treatment enhanced the expression of genes encoding enzymes for jasmonic acid biosynthesis (Fig. 6.3; Méndez-Bravo et al. 2011). It enhanced the expression of lipoxygenase genes (LOX2 and LOX3), allene oxide synthase gene (AOS), allene oxide cyclase2 gene (AOC2), and OPDA reductase3 (OPR3) gene (Méndez-Bravo et al. 2011). The N-isobutyl decanamide treatment increased JA accumulation in Arabidopsis seedlings (Méndez-Bravo et al. 2011). The alkamide treatment induced the expression of the JA-inducible genes JAZ8, VSP2 and ERF2. Expression of these genes was repressed in the JA insensitive Arabidopsis mutant coronatine insensitive1 (coi1-1). These results suggest that the alkamide activates the JA biosynthesis and signaling pathway. The alkamide was ineffective in conferring resistance against the necrotrophic pathogen Botrytis cinerea in Arabidopsis mutants jar1 and coi1, which are altered in JA signaling (Méndez-Bravo et al. 2011). The alkamide was also unable to confer resistance against B. cinerea in an Arabidopsis MAP kinase mutant (mpk6) (MéndezBravo et al. 2011). MPK6 is known to activate several transcriptional regulators, such as members of the WRKY, MYC and ERF gene families when it is phosphorylated. MPK6 functions as substrate of four MAPK kinases (MKK2, MKK3, MKK4 and MKK5). The MKK3-MPK6 cascade is activated in response to JA and both, positively and negatively regulates the expression of JA-related genes (Takahashi et al. 2007; Hu et al. 2009). The MKK3-MPK6 is an important part of the jasmonatesignal transduction pathway (Takahashi et al. 2007). The inability of the alkamide to induce defense responses in mpk6 mutant suggests the involvement of JA signaling system in alkamide-induced resistance (Méndez-Bravo et al. 2011). In contrast, the alkamide was effective in controlling the disease caused by B. cinerea in the Arabidopsis salicylic acid (SA)-related mutant eds16/sid2-1, similar to wild-type plants (Méndez-Bravo et al. 2011). Collectively these results suggest that the alkamideinduced resistance depends on activation of JA signaling system and SA signaling system may not have any role in induction of disease resistance. The alkamide treatment induces resistance against Botrytis cinerea infection in Arabidopsis. It reduced the disease incidence (Fig. 6.4; Méndez-Bravo et al. 2011). It also reduced the intensity of lesion development. The results suggest that the alkamide has great potential to combat pathogens by triggering JA biosynthesis pathway.

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Linolenic acid

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Increases expression of LOX2, LOX3 genes

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N-isobutyl decanamide

Increase in OPDA reductase 3 enzyme activity

Increase in JA accumulation

Fig. 6.3 Increased expression of genes encoding JA biosynthesis enzymes induced by N-isobutyl decanamide (Adapted from Méndez-Bravo et al. 2011)

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120 100 80

Symptomatic leaves (%)

60 40 20 0 Control

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Fig. 6.4 Induced resistance against Botrytis cinerea by alkamide treatment in Arabidopsis thaliana (Adapted from Méndez-Bravo et al. 2011)

6.4 Molecular Manipulation of Lipoxygenase Enzyme Involved in JA Biosynthesis by Chitosan for Crop Disease Management Chitosan (β-1,4-linked glucosamine), a deacetylated derivative of chitin has been developed as a potential activator of JA signaling system to induce defense responses for crop disease management (Bueter et al. 2013; Vidhyasekaran 2014, 2015). Chitosan triggers activity of lipoxygenase, the key enzyme in JA biosynthetic pathway, in several crop plants. Chitosan triggers lipoxygenase activity in wheat (Bohland et al. 1997; Jayaraj et al. 2009). Chitosan treatment induces octadecanoid signaling system, resulting in increased accumulation of JA in rice (Rakwal et al. 2002). Chitosan treatment induced accumulation of jasmonic acid in tomato leaves (Fig. 6.5; Doares et al. 1995). These results suggest that chitosan may function through JA signaling system. Several chitosan formulations have been developed for management of crop diseases. A commercial formulation of chitosan has been developed by Glycogene Sys Inc. (Boston) under the trade name ‘Elexa’. It protects a range of crops against several pathogens. Ecobulle, France developed chitosan as a commercial product under the trade name Chitogel (Elmer and Reglinski 2006). Another formulation containing 4% chitosan has been developed as “Elexa 4 Plant Defense Booster” by Plant Defense Boosters Inc. USA (Elmer and Reglinski 2006). ChiPro GmbH, Bremen, Germany developed the chitosan formulation under the trade name ChitaPlant® . ´ Biochikol is another commercial formulation of chitosan (Kurzawiηska and Mazur 2009). “Chitoplant” is the commercial product sold as a plant strengthener in Germany (Dafermos et al. 2012). A chitosan formulation based on a 4% chitosan with 1.5% Cu2+ and 0.5% Mn under the trade name Kendal Cops® has been developed (Iriti et al. 2011).

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JA (pmol/g) 150 100 50 0 Control

Chitosan

Fig. 6.5 Increases in intracellular levels of JA in leaves of tomato plants in response to chitosan treatment (Adapted from Doares et al. 1995)

Chitosan activates plant innate immune system and controls several crop diseases. It is effective in controlling various Fusarium diseases in tomato (Benhamou 1992; Benhamou and Thériault 1992; Benhamou et al. 1994, 1998; Lafontaine and Benhamou 1996), wheat (Reddy et al. 1999), soybean (Prapagdee et al. 2007), potato (Li et al. 2009), and celery (Bell et al. 1998). Chitosan triggers defense responses against various powdery mildew pathogens in tomato (Gorbatenko et al. 1996; Isebaert et al. 2002; Dafermos et al. 2012), cucumber (Moret et al. 2009), grapevine (Gorbatenko et al. 1996; Iriti et al. 2011) and barley (Faoro et al. 2008). Chitosan triggers resistance against Botrytis cinerea infection in grapevine (Romanazzi et al. 2002; Ait Barka et al. 2004; Amborabé et al. 2004; Elmer and Reglinski 2006), tomato (Liu et al. 2007), and carrot (Jayaraj et al. 2009). Chitosan induces resistance against several oomycete pathogens (Sharathchandra et al. 2004; Aziz et al. 2006). Chitosan also induces resistance against several virus diseases (Zhao et al. 2007; Hu et al. 2008; Iriti and Faoro 2008, 2009; Hu et al. 2009). Chitosan appears to be a useful tool to manage crop diseases without any sacrifice in the crop yield potential.

6.5 Bioengineering for Production of Arachidonic Acid in Plants to Activate JA Biosynthesis Pathway Genes for Disease Management Arachidonic acid (5,8,11,14-cis-eicosatetraenoic acid) is an elicitor of plant defense responses. It is found in oomycetes (Bostock et al. 1981, 1986, 1992; Creamer and Bostock 1988; Vidhyasekaran 2007a) and fungi (Eroshin et al. 2000). Exogenous application of arachidonic acid-containing preparation from the fungus Mortierella hygrophila reduced the development of late blight, common scab, and rhizoctonia diseases in potato (Eroshin and Dedyukhina 2002). This preparation also reduced the

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development of cercospora disease in sugar beet and powdery mildew in grapevine (Eroshin and Dedyukhina 2002). Arachidonic acid preparation induced resistance against the oomycete pathogen Phytophthora infestans, the fungal pathogens Alternaria solani and Septoria lycopersici, and the bacterial pathogen Xanthomonas vesicatoria in tomato (Ozeretskovskaya et al. 2004). Arachidonic acid treatment induced resistance against Tobacco mosaic virus in tobacco (Rozhnova et al. 2003). These studies suggest that arachidonic acid can be used as a tool for management of oomycete, fungal, bacterial and viral diseases in various crop plants by triggering plant defense system. However, arachidonic acid is not commonly found in higher plants (Dedyukhina et al. 2014). It is abundant in Phytopthora species and other oomycetes (Ricker and Bostock 1992). It is released from spores into plants during early stages of infection by oomycete pathogens (Ricker and Bostock 1992; Savchenko et al. 2010). Potato leaves were inoculated with two different races of the late blight pathogen Phytopthora infestans. Release of the elicitor from sporangia of P infestans into the compatible race-inoculated potato leaf tissues was observed at 12 h after inoculation, while it was observed at 9 h in the incompatible interaction. The only difference between susceptible and resistant reactions was a 3 h delay in release of elicitor in the former interaction (Ricker and Bostock 1992). The results suggest that if arachidonic acid is made available at the site of infection during the initiation of the infection process stage itself, the disease can be effectively controlled (Vidhyasekaran 2007a). Bioengineering technology has been developed to make the plants themselves to produce arachidonic acid without any pathogen invasion (Qi et al. 2004). Production of arachidonic acid in a higher plant was achieved using genes encoding enzymes participating in the 8 -desaturation biosynthetic pathways for the formation of C20 polyunsaturated fatty acids. Arabidopsis thaliana was transformed sequentially with genes encoding a 9 -specific elongating activity from an alga, Isochrysis galbana, a 8 -desaturase from a unicellular flagellate organism, Euglena gracilis and a 5 desaturase from a fungus, Mortierella alpina (Qi et al. 2004; Savchenko et al. 2010). While the wild-type plants did not contain arachidonic acid, the transgenic plants contained easily detectable levels of arachidonic acid (Savchenko et al. 2010). The arachidonic acid-containing transgenic plants showed increased levels of jasmonic acid. The increased levels of jasmonic acid correlated with enhanced expression of genes encoding enzymes involved in the jasmonate biosynthetic pathway. The transgenic plants showed increased expression of DGL gene encoding phospholipase A (Fig. 6.6; Savchenko et al. 2010). Phospholipase A releases linolenic acid from membrane and the linolenic acid is oxygenated by lipoxygenases to produce hydroperoxide derivatives in the JA biosynthetic pathway (see Fig. 6.1). The transgenic plants showed enhanced expression of LOX3 gene encoding lipoxygenase and AOS gene encoding allene oxide synthase (Fig. 6.7; Savchenko et al. 2010). The transgenic plants showing elevated levels of JA showed enhanced resistance to the fungal pathogen Botrytis cinerea and the oomycete pathogen Phytophthora capsici (Savchenko et al. 2010). These results suggest that developing transgenic plants constitutively producing arachidonic acid may be a potential approach to activate JA pathway for management of plant diseases.

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Relative expression of phospholipase A gene (DGL)

0.5 0.4 0.3 0.2 0.1 0 Wild-type plants

Transgenic plants

Fig. 6.6 Enhanced expression of DGL gene encoding phospholipase A in transgenic Arabidopsis plants producing arachidonic acid (Adapted from Savchenko et al. 2010)

Fig. 6.7 Enhanced expression of lipoxygenase (LOX3) and allene oxide synthase (AOS) genes in transgenic Arabidopsis plants producing arachidonic acid (Adapted from Savchenko et al. 2010)

3 2.5 2

Relative expression

Wild-type plants

1.5

Transgenic plants

1 0.5 0 LOX3

AOS

6.6 Manipulaion of JA-Dependent Signaling System Using Hexanoic Acid for Plant Disease Management Hexanoic acid is a nine carbon dicarboxylic acid that acts as an inducer of plant defenses by means of a priming mechanism (Vicedo et al. 2009). Priming results in a faster and stronger induction of defense mechanisms after pathogen attack (Conrath 2011; Po-Wen et al. 2013). Hexanoic acid treatment primes tomato plants against the bacterial pathogen Pseudomons syringae pv. tomato and the fungal pathogen Botrytis cinerea (Vicedo et al. 2009). Hexanoic acid treatment induced LoxD mRNA accumulation 72 h after inoculation with the fungal pathogen B. cinerea in tomato leaves but no differences were observed in the absence of infection (Vicedo et al. 2009). The gene LoxD encodes lipoxygenase, a key enzyme in JA biosynthesis pathway. 12-oxo-phytodienoic acid (OPDA), a precursor of JA, accumulated in tomato plants

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in response to B. cinerea inoculation and hexanoic treatment raised the OPDA levels 72 h after fungal infection. JA-conjugate JA-Ile accumulated 48 h after B. cinerea inoculation and the level of JA-Ile further increased after hexanoic acid treatment (Vicedo et al. 2009). The results suggest that hexanoic acid primes JA biosynthesis pathway. The importance of hexanoic acid in inducing JA signaling system-dependent defense reponses has been demonstrated in tomato (Vicedo et al. 2009) and Arabidopsis (Kravchuk et al. 2011). The tomato coi1 homolog jasmonate-insensitive jai1 mutant and wild-type plants were treated with hexanoic acid and 48 h after treatment the plants were infected with Botrytis cinerea. Hexanoic acid treatment increased resistance to the pathogen in wild-type plants but had no effect on jai mutant plants (Vicedo et al. 2009). The results suggest that COI1-dependent JA signaling is involved in hexanoic acid-induced resistance against B. cinerea. JA signaling pathway showed dramatic changes after hexanoic acid treatment in Arabidopsis, mainly when the pathogen B. cinerea was inoculated (Kravchuk et al. 2011). The impaired JA mutants, jin1-2 and jar1, were unable to display hexanoic acid-induced priming against B. cinerea. Hexanoic acid-treated plants infected with B. cinerea showed priming in the expression of the PDF1.2, PR-4 and VSP1 genes implicated in the JA pathways. JA and OPDA levels were primed at early stages by hexanoic acid (Kravchuk et al. 2011). These results suggest that hexanoic acid induces JA-dependent defense responses by priming in Arabidopsis (Kravchuk et al. 2011). Hexanoic acid treatment protects tomato plants against B. cinerea infection (Leyva et al. 2008; Vicedo et al. 2009). It also effectively controlled Pseudomonas syringae infection in tomato (Vicedo et al. 2009). Hexanoic acid has been reported to be a potent natural priming agent of proven efficacy in a wide range of host plants and pathogens (Aranega-Bou et al. 2014). Hexanoic acid has priming effect through activation of genes involved in the establishment of systemic acquired resistance (Djami-Tchatchou et al. 2017). Priming for JA-dependent defenses using hexanoic acid appears to be an effective tool for management of crop diseases.

6.7 Manipulation of Jasmonic Acid Signaling Pathway Using Ulvan for Crop Disease Management Ulvan is a plant defense activator. It is a sulfated polysaccharide product isolated from green algae belonging to the Ulva genus (Jaulneau et al. 2010). The main constituents of uvan are sulfated rhamnose residues linked to uronic acids, resulting in ` a repeated disaccharide unit β-D-glucuronosyl-(1,4)-α-L-rhamnose 3-sulfate, called aldobiouronic acid (Lahaye and Robic 2007). Ulvan treatment induced elevation of JA content in Medicago truncatula. It also induced the expression of well-known jasmonic acid-responsive genes including lipoxygenase, hydroxyproline-rich glycoproteins, proline-rich proteins, defensin and

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wound-induced protein (Jaulneau et al. 2010). Trypsin inhibitory activity was also induced in ulvan-treated M. truncatula leaves (Jaulneau et al. 2010) and the induction of trypsin inhibitory activity is the typical plant response to JA (Ryan 2000). Ulvan treatment strongly induced the expression of PDF1.2, a JA-responsive defensin gene in Arabidopsis thaliana (Jaulneau et al. 2010). The elicitor activity of ulvan was shown to be dependent on JAR1 (Jasmonate resistant 1) in A. thaliana. JAR1 is a JA-amino acid synthase and activates conjugation of JA to an amino acid and this enzyme may be involved in Jasmonoyl-isoleucine, (JA-Ile) biosynthesis (Staswick and Tiryaki 2004). JA-Ile has been shown to be involved in defense signaling (Katsir et al. 2008; Gfeller et al. 2010; Kombrink 2012; Wasternack and Hause 2013). These results suggest that ulvan is a potential elicitor of defense responses and it acts by enhancing the activity of JA signaling system. Ulva extract containing ulvan effectively controlled the infection by Colletotrichum trifolii in Medicago truncatula (Cluzet et al. 2004). Foliar spraying of ulvan reduced severity of anthracnose disease caused by Colletotrichum lindemuthianum in bean (de Freitas and Stadnik 2012). Ulvan treatment induces resistance against Alternaria brassicicola and Colletotrichum higginsianum in Arabidopsis thaliana (de Freitas and Stadnik 2015; de Freitas et al. 2015). Ulvan induced resistance against the rust pathogen Uromyces appendiculatus in bean (Delgado et al. 2013). Ulva spp. are common on all seashores and they can produce in time an important amount of biomass in nutrient-enriched waters. Hence ulvan derived from the green algae may be a powerful tool to manage crop diseases (Lahaye and Robic 2007).

6.8 Engineering Transcription Factor Genes to Manipulate JA Signaling System for Crop Disease Management MYC2 is a nuclear localized basic helix-loop-helix-leucine zipper – type transcription factor (Boter et al. 2004; Lorenzo et al. 2004; Wager and Browse 2012; Vidhyasekaran 2016). It plays an important role in transduction of JA signals to trigger biosynthesis of PR proteins and several defense-related secondary metabolites (Kazan and Manners 2013; Zhang et al. 2018). It plays a predominant role in JA signaling pathway, activating transcription of the JA-responsive PDF1.2 encoding the PR-12 defensin protein (Lorenzo and Solano 2005; Takahashi et al. 2007). MYC2 positively regulates the JA-responsive genes VSP and LOX (Lorenzo et al. 2004; Pozo et al. 2004). MYC2 acts as a master switch that regulates JA-mediated biosynthesis of secondary metabolites (Kazan and Manners 2013). MYC2 is involved in the transcriptional regulation of JA-responsive gene expression (Lorenzo et al. 2004; Chini et al. 2007). MYC2 interacts with JAZ proteins and mediate JA responses. In the absence of a JA signal, JAZ proteins repress MYC2. Upon sensing of the JA signals, JAZ repressors are recruited to the SCF E3 complex for ubiquitination and subsequent degradation by the proteasome. The removal of

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these repressors then paves the way for MYC2 to regulate JA-dependent gene expression (Lorenzo et al. 2004; Chini et al. 2007, 2009; Gfeller et al. 2010; Wager and Browse 2012; Vidhyasekaran 2015). JAZs function as inhibitors of the transcription factor that, when free of JAZ inhibition, act to activate transcription from JA-response genes (Wager and Browse 2012). The nuclear targeting of JAZ1 and JAZ9 has been shown to be dependent on physical interaction with MYC2 via a highly conserved region of the Jas domain (Withers et al. 2012). OsMYC2, the rice homolog of the Arabidopsis MYC2, AtMYC2, has been cloned (Cai et al. 2014; Uji et al. 2016). Transgenic rice plants overexpressing OsMYC2 have been developed (Uji et al. 2016). OsMYC2 from rice selectively binds to the G-box-like motif of the OsJAZ10 promoter in vivo and regulates the expression of JAresponsive genes in rice (Uji et al. 2016). The transgenic rice plants overexpressing OsMYC2 showed resistance against the rice bacterial blight pathogen Xanthomonas oryzae pv.oryzae (Uji et al. 2016). The results suggest that MYC2 gene can be used for engineering to develop disease resistant plants. The transcription factor gene, VvWRKY1, isolated from Vitis vinifera were used to develop transgenic grapevine plants. The transgenic plants showed increased expression of two lipoxygenase genes (LOXO and LOXA) involved in JA biosynthesis and two genes encoding proteins similar to JAZ1 and JAZ2, which are transcriptional repressors in JA signaling system (Marchive et al. 2013). The transgenic plants showed resistance to the downy mildew pathogen Plasmopara viticola (Marchive et al. 2013). The results suggest that VvWRKY1 can be engineered to enhance the expression of genes involved in the JA signaling system resulting in activation of plant defense responses and the transcription factor gene is a potential tool to develop downy mildew-resistant grapevine variety.

6.9 Manipulation of JA Signaling System Using Microbes for Crop Disease Management 6.9.1 Trichoderma asperellum Trichoderma spp. are known to be involved in triggering ‘induced systemic resistance’ (ISR) in many plants (Harman et al. 2004; Vidhyasekaran 2004; Shoresh et al. 2010; Mathys et al. 2012; Martinez-Medina et al. 2013; Harel et al. 2014). Application of Trichoderma asperellum T 203 to the root system of cucumber plants induced systemic resistance against the foliar bacterial pathogen Pseudomonas syringae pv. lachrymans and reduced the angular leaf spot symptom development (Yedidia et al. 2003). The Trichoderma strain induced the expression of Lox1 encoding lipoxygenase (LOX), the key enzyme in LOX pathway which is involved in biosynthesis of JA (Shoresh et al. 2005). It also induced the lipoxygenase pathway gene encoding hydroperoxide lyase (HPL) (Yedidia et al. 2003). The lipoxygenase pathway is

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involved in JA signaling system (Vidhyasekaran 2015). Application of a JA production inhibitor (diethyldithiocarbamic acid, DIECA) strongly inhibited or completely abolished the protective effect of T. asperellum T203 on plants (Shoresh et al. 2005). These studies suggest that T. asperellum T 203 controls plant diseases by inducing JA signaling system.

6.9.2 Trichoderma virens Trichoderma virens is a commercially formulated biocontrol agent and it is effective in the control of Rhizoctonia solani, Sclerotium rolfsii, and Pythium spp in several crop plants (Mukherjee and Kenerley 2010). It induces resistance against several crop diseases by activating JA signaling system. T. virens GV29-8 strain induced ISR in maize against Colletotrichum graminicola (Djonovic et al. 2007). Allene oxide synthase (AOS) is the key enzyme in lipoxygenase (LOX) pathway, which is involved in JA biosynthesis. AOS gene was up-regulated by T. virens (Djonovic et al. 2007). Another gene from the JA biosynthetic pathway up-regulated by T. virens GV29-8 is OPR7 encoding 12-oxo-phytodienoic acid reductase (Fig. 6.8; Djonovic et al. 2007). The results suggest that application of T. virens activates JA biosynthetic pathway- dependent defense system and induces disease resistance.

6.9.3 Trichoderma harzianum Trichoderma harzianum is the commonly used and most effective biocontrol agent commercially available for use against a wide variety of plant diseases (Elad et al. 1998; Elad 2000a, b; Etebarian et al. 2000; Jung et al. 2009; Perazzolli et al. 2008, 2011; Tucci et al. 2011; Moran-Diez et al. 2012; Harel et al. 2014; Martinez-Medina et al. 2013, 2014). T. harzianum induces systemic resistance against pathogens. It has been shown that T. harzianum induces systemic resistance against Botrytis cinerea in tomato mostly through a boosted JA-dependent defense response (Martinez-Medina et al. 2013).

6.9.4 Pseudomonas putida BTP1 Several rhizobacterial strains trigger the plant immune response by activating JA signaling system. Pseudomonas putida strain BTP1 treatment primes tomato plants to activate two key enzymes (Djonovic et al. 2006, 2007) of lipoxygenase (LOX) pathway, lipoxygenase (LOX) and lipid hydroperoxidase (LHP) after challenge inoculation with the pathogen Botrytis cinerea (Akram et al. 2008). The increase in the enzyme activities was observed only after challenge by the pathogen and this priming effect appears to be almost invariably associated with the ISR phenomenon.

6.9 Manipulation of JA Signaling System Using Microbes …

239 Linolenic acid

Lipoxygenase

13 S-hydroperoxy octadecatrienoic acid

acƟvates

Allene oxide synthase

Trichoderma virens

12,13 epoxy-octadecatrienoicacid

Allene oxide cyclase 12-oxo-phytodienoic acid (OPDA)

OPDA reductase 3-oxo-2-2’-(Z-pentenyl) cyclopentane1-octanoicacid (OPC 8:0)

Jasmonic acid

Fig. 6.8 Enzymes upregulated by Trichoderma virens in the JA biosynthesis pathway. (Adapted from Djonovic et al. 2007)

The LOX pathway is involved in the JA signaling system (Delker et al. 2007; Vidhyasekaran 2007a; Balbi and Devoto 2008), suggesting the role of JA signaling in the P. putida BTP1-induced resistance. P. putida BTP1 induces ISR in bean against the gray mold pathogen B. cinerea (Ongena et al. 2002) and in cucumber against the root rot oomycete pathogen Pythium aphanidermatum (Ongena et al. 1999, 2000). It also activates the plant immune system in Arabidopsis and induces resistance against the bacterial pathogen Pseudomonas syringae pv. tomato (Ramos Solano et al. 2008).

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Chapter 7

Bioengineering and Molecular Manipulation of Ethylene Signaling System for Crop Disease Management

Abstract Ethylene signaling system is one of the most important signaling systems which can activate plant innate immunity. This system can be manipulated for inducing systemic resistance (ISR) against fungal, oomycete, bacterial and viral pathogens. Under natural conditions endogenous ethylene content is very low and its level can be increased using several molecular techniques. Increase in ethylene biosynthesis may induce enhanced defense responses. Hence several attempts were made to induce ethylene biosynthesis in plants for disease management. Transgenic rice lines overexpressing ACC synthase gene, OsACS2, have been generated and these transgenic plants show increased levels of endogenous ethylene. The transgenic lines overexpressing OsACS2 show increased resistance to the rice blast pathogen Magnaporthe oryzae and the rice sheath blight pathogen Rhizoctonia solani. ERF belonging to the APETELA2 (AP2)/ETHYLENE RESPONSIVE ELEMENT BINDING PROTEIN (EREBP) transcription factor family is the important group of transcription factors functioning downstream in ethylene signaling system. Several attempts have been made to develop transgenic plants using ERF genes from different plants. An ERF transcription factor gene, GbERF2, was cloned from cotton and used to develop transgenic tobacco plants for management of tobacco diseases. The transgenic tobacco plants constitutively accumulate high levels of transcripts of PR-1b, PR2, and PR4 genes. These plants show enhanced resistance to the necrotrophic fungal pathogen Alternaria longipes. Transgenic tobacco plants overexpressing the rice OsBIERF3 gene have been developed. The transgenic tobacco plants show enhanced resistance against both viral and bacterial pathogens. Transgenic tobacco plants expressing tobacco Tsi1 gene encoding an EREBP-AP2-type transcription factor show enhanced resistance against Pseudomonas syringae pv. tabaci. The transgenic hot pepper plants expressing the tobacco Tsi1 exhibit resistance to Pepper mild mottle virus, Cucumber mosaic virus, Xanthomonas campestris pv. vesicatoria and Phytophthora capsici. ERF1-V, an ethylene-responsive element-factor gene of the AP2/ERF transcription factor gene family was cloned from Haynaldia villosa, a wild species of wheat. Transgenic wheat plants overexpressing EFR1-V show enhanced resistance to the powdery mildew pathogen Blumeria graminis f. sp. tritici. EIN2 is a membrane protein that acts as the central regulator of ethylene signaling pathways. The rice plants overexpressing OsEIN2 show enhanced resistance against the rice blast pathogen © Springer Nature B.V. 2020 P. Vidhyasekaran, Plant Innate Immunity Signals and Signaling Systems, Signaling and Communication in Plants, https://doi.org/10.1007/978-94-024-1940-5_7

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Magnaporthe oryzae. Ethylene signaling system can be activated by using different rhizobacteria. Pseudomonas fluorescens WCS417r induces systemic resistance (ISR) in plants. It activates the transcription factor MYB72 and the activated MYB72 gene interacts with EIL3 transcription factor, resulting in activation of ET signaling system. Trichoderma asperellum triggers ISR against several pathogens. Ethylene signal transduction pathway has been shown to be involved in the ISR induced by T. asperellum. The major action of Trichoderma appears to be suppression of the action of both ETR1 and CTR1, the negative regulators of ethylene signaling. Pythium oligandrum treatment induces disease resistance against several pathogens. It induces biosynthesis of ethylene in plants. It also activates ethylene signaling pathway. Activation of the ethylene-dependent signaling pathway was accompanied by increased expression of genes encoding ethylene receptors and ethylene-responsive transcription factors. Keywords ACC synthase gene · ERF transcription factor gene · EIN gene · Pseudomonas · MYB2 gene · Trichoderma · ETR1 · CTR1 · Negative regulators of ethylene signaling

7.1 Ethylene Signaling System Triggers Local and Induced Systemic Resistance Ethylene (ET) signaling system is an important component in plant defense system (Chen et al. 2003; Cao et al. 2006; Iwai et al. 2006; van Loon et al. 2006; Xu et al. 2007; Lin et al. 2008; Berr et al. 2010; Nie et al. 2011; Akagi et al. 2011; Sun et al. 2012; Helliwell et al. 2013; Shakeel et al. 2013; Vidhyasekaran 2014, 2015; Yang et al. 2017; Shima et al. 2018). Ethylene has been considered as a modulator of disease resistance in plants (van Loon et al. 2006). ET signaling system has been shown to induce resistance against the necrotrophic fungal pathogen Botrytis cinerea in Arabidopsis (Geraats et al. 2003; Moffat et al. 2012), apple (Akagi et al. 2011), and tomato (Nambeesan et al. 2012). ET signaling pathway is involved in inducing resistance against the rice blast pathogen Magnaporthe oryzae (Iwai et al. 2006; De Vleesschauwer et al. 2008). Activation of ethylene signaling system has been shown to be indispensable for resistance to the rice blast pathogen M. oryzae (Yang et al. 2017). Ethylene induced partial resistance in Medicago truncatula against the charcoal rot pathogen Macrophomina phaseolina (Gaige et al. 2010). Ethylene induces systemic resistance against Turnip mosaic virus (TuMV) infection in leafy mustard plants (Zhu et al. 2011). Ethylene signaling system plays an important role in induced systemic resistance (ISR) triggered by microbes (Van Peer et al. 1991; Meziane et al. 2005; Shoresh et al. 2005; Korolev et al. 2008; Vidhyasekaran 2015).

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7.2 Molecular Manipulation of Ethylene Biosynthesis Pathway for Crop Disease Management Under natural conditions endogenous ethylene content is very low and its level increases only under stress conditions (Vidhyasekaran 2015; Ravanbakhsh et al. 2018). Pathogen infection (Chen et al. 2003; Akagi et al. 2011; Helliwell et al. 2013), and biotic (Hase et al. 2006; Takahashi et al. 2006) or abiotic elicitor treatments (Harel et al. 2014) induce enhanced ethylene biosynthesis and an increase in endogenous ethylene content. Increase in ethylene biosynthesis may induce enhanced defense responses (Hase et al. 2006; Helliwell et al. 2013; Harel et al. 2014). Hence several attempts were made to induce ethylene biosynthesis in plants for disease management. Transgenic rice lines with inducible production of ethylene were generated by expressing the rice ACS2 (1-aminocyclopropane-1-carboxylic acid synthase, a key enzyme of ethylene biosynthesis) transgene under control of a strong pathogeninducible promoter (Helliwell et al. 2013). In comparison with the wild-type plant, the OsACS2-overexpression lines showed significantly increased levels of the OsACS2 transcripts, endogenous ethylene and defense gene expression, especially in response to pathogen infection (Fig. 7.1; Helliwell et al. 2013). The transgenic lines overexpressing OsACS2 exhibited increased resistance to the rice blast pathogen Magnaporthe oryzae (Fig. 7.2; Helliwell et al. 2013). The transgenic plants also showed resistance to the rice sheath blight pathogen Rhizoctonia solani. Assessment of the plant growth rate and seed production revealed little or no differences between wild type and transgenic lines. The results suggest that pathogen-inducible production of ethylene in transgenic rice can enhance resistance to necrotrophic and hemibiotrophic fungal pathogens without negatively impacting crop productivity (Helliwell et al. 2013).

7.3 Engineering ERF Genes to Manipulate Ethylene Signaling System for Crop Disease Management Ethylene (ET) signaling system plays important role in inducing defense genes (Ohme-Takagi and Shinshi 1995; Penninckx et al. 1998; Park et al. 2001; Díaz et al. 2002; Cao et al. 2006; Lin et al. 2008; Akagi et al. 2011; Kim et al. 2011; Vidhyasekaran 2015). Plants under stress produce increased levels of ethylene. The increase in ethylene coincides with an increase in 1-aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS) activity, which is followed by ACC oxidase activity. After increase in ethylene production, a strong activation of ETHYLENE-RESPONSE FACTOR (ERF) genes is observed (Kim et al. 2011). In Arabidopsis, ethylene is perceived by a family of five membrane-bound receptors (ETR1, ERS1, ETR2, EIN4, and ERS2), which transmit the signal to downstream effectors (Wang et al. 2006). In all the receptors, the predicted transmembrane domain

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L-Methionine Engineering OsACS2 gene in rice plants

S-adenosyl methionine (S-AdoMet)

Increased levels of OsACS2 transcripts

Overexpression of ACC synthase (ACS) 1-aminocyclopropane-1carboxylic acid (ACC) ACC oxidase (ACO) Overproduction of ethylene

Overexpression of defense genes Fig. 7.1 Overexpression of OsACS2 gene triggers overproduction of ethylene in rice plsnts (Adapted from Helliwell et al. 2013) 35 30 25

Lesion number per leaf

20 15 10 5 0 Wild-type plants

Transgenic plants expressing OsACS2

Fig. 7.2 Increased resistance of OsACS2–overexpressing rice plants to the rice blast pathogen Magnaporthe oryzae (Adapted from Helliwell et al. 2013)

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at the N terminus comprises the ethylene binding domain (EBD). The C-terminal half of the receptors consists of a His kinase domain and in some cases, a receiver domain (ETR1, ETR2. and EIN4). The five receptors are classified into two subfamilies: subfamily 1 (ETR1 and ERS1) and subfamily 11 (ETR2, EIN4, and ERS2) (Wang et al. 2006). The subfamily I receptors are capable of His kinase activity, while subfamily II members and ERS1 have Ser/Thr kinase activity. These observations suggest ethylene binding results in an alteration in the signaling state of the cytoplasmic transmitter domains of the receptors (Wang et al. 2006). In the absence of ethylene, ethylene receptors act as negative regulators and activate CTR1, Raf-like serine/threonine kinase that phosphorylates an ER-located membrane protein EIN2 to repress ethylene signaling (Kieber et al. 1993). The presence of ethylene switches off CTR1, leading to activation of positive regulators EIN2 and EIN3 (Chao et al. 1997). EIN2 is cleaved, releasing the C-terminal fragment, which moves to the nucleus and stabilizes EIN3 and EIN3-Like 1 (EIL1) by downregulating EIN3-binding F-box protein 1 (EBF1) and EBF2 required for EIN3/EIL1 degradation (Ju et al. 2012; Qiao et al. 2012; Wen et al. 2012). EIN3 and EIL1 then regulate the expression of ERF-family transcription factors (Solano et al. 1998). Functional studies of EIN3 have shown that EIN3 can bind to the promoter sequence of the ethylene inducible transcription factor ERF1 in Arabidopsis (Fig. 7.3; Solano et al. 1998). EIN3 indirectly induces defense-related genes via transcriptional activation of ERF1. In turn, ERF1 interacts with the GCC box motif in promoter regions of ethylene-regulated defense genes in Arabidopsis (Solano et al. 1998). ERF genes encode one AP2/ERF domain composed of three β-sheets and one α-helix; the β-sheets interact with the GCC-box motif in the target DNA (Allen et al. 1998). Analysis of several basic PR genes indicate that an 11-bp consensus sequence (TAAGAGCCGCC) with the core sequence of AGCCGCC known as GCC box) is required for the ethylene responses (Ohme-Takagi and Shinshi 1995). These ethylene-responsive AP2/EREBP genes have a conserved basic 58 or 59-amino acid DNA-binding domain and function as regulators of GCC box mediated transcription of defense genes (Ohme-Takagi and Shinshi 1995; Akagi et al. 2011). ERFs have been shown to bind specifically to the GCC box that is found in several promoters of the pathogenesis-related (PR) genes (Yamamoto et al. 1999; Gutterson and Reuber 2004). ERF belonging to the APETELA2 (AP2)/ETHYLENE RESPONSIVE ELEMENT BINDING PROTEIN (EREBP) transcription factor family is the important group of transcription factors functioning downstream in ethylene signaling system (Gutterson and Reuber 2004; Grennan 2008; Vidhyasekaran 2016). In Arabidopsis, 147 members of the AP2/EREBP gene family have been detected (Feng et al. 2005). The AP2/EREBP family is divided into the RAV, AP2, and EREBP subfamilies. The EREBP subfamily is further divided into DREB or A subgroup and the ERF or B subgroup. The ERF subgroup contains 65 ERF genes and contains all of the AP2/EREB genes that have been linked to disease resistance responses (Gutterson and Reuber 2004). The important ERF transcription factors involved in defense signaling system include AtERF1, AtERF2, AtERF4, AtERF14, and ORA59 in Arabidopsis (McGrath et al. 2005; Grennan 2008; Kim et al. 2018), ERF2, ERF3, and ERF4 in tobacco (Koyama et al. 2003), ERF2 and ERF4 in canola (Brassica napus)

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Ethylene

activation EIN2 activation EIN3

Binds with promoter sequence of ERF1

Transcriptional activation of ERF1

Binds with GCC box motif in promoter region in PR genes

Activation of PR genes Fig. 7.3 Activation of PR genes by ERF gene. Activation of genes by gene (Adapted from Solano et al. 1998)

(Yang et al. 2007), TaERF1 and TaERF3 in wheat (Xu et al. 2007; Zhang et al. 2007), CaPF1 and CaERFLP 1 in pepper (Lee et al. 2004; Yi et al. 2004), OsBIERF3 in rice (Cao et al. 2006), Pti4 and Pti5 in tomato (Zhou et al. 1997), and HvRAF in barley (Jung et al. 2007). Several attempts have been made to develop transgenic plants using ERF genes from different plants. An ERF transcription factor gene, GbERF2, was cloned from cotton and used to develop transgenic tobacco plants for management of tobacco

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90 80 70 60

Disease 50 index 40 30 20 10 0 Wild-type plants

Transgenic plants

Fig. 7.4 Enhanced disease resistance against Pseudomonas syringae pv. tabaci in OsBIERF3overexpressing tobacco (Adapted from Cao et al. 2006)

diseases (Zuo et al. 2007). The transgenic tobacco plants constitutively accumulated high levels of transcripts of PR-1b, PR2, and PR4 genes. These plants showed enhanced resistance to the necrotrophic fungal pathogen Alternaria longipes (Zuo et al. 2007). Transgenic tobacco plants overexpressing the rice OsBIERF3 gene were developed by Agrobacterium-mediated leaf disc transformation with a construct containing OsBIERF3 ORF under control of the cauliflower mosaic virus 35S promoter (Cao et al. 2006). Overexpression of the rice OsBIERF3 gene in tobacco showed enhanced expression of the defense-related PR-1a gene with GCC box in its promoter. Coincidence between the PR-1a expression level and the OsBIERF3 mRNA amount in the OsBIERF3-overexpressing transgenic plants was observed. The transgenic tobacco plants showed enhanced resistance against the bacterial pathogen Pseudomonas syringae pv. tabaci, the causal agent of wild fire disease in tobacco (Fig. 7.4; Cao et al. 2006). These transgenic tobacco plants also showed resistance against Tomato mosaic virus (Cao et al. 2006). Transgenic tobacco plants expressing tobacco Tsi1 gene encoding an EREBPAP2-type transcription factor showed enhanced resistance against P. syringae pv. tabaci. The expression of the pathogenesis-related proteins PR1and PR2, osmotin, and SAR8.2 was high in the Tsi1-overexpressing transgenic tobacco plants (Park et al. 2001). NtERF5, a member of the tobacco AP2/ERF transcription factor family, has been cloned and transgenic tobacco plants expressing this gene were developed (Fischer and Dröge-Laser 2004). Constitutive overexpression of NtERF5 gene under control of the 35S promoter showed enhanced resistance to Tobacco mosaic virus (TMV). In TMV-infected ERF5-overexpressing plants, the viral RNA accumulated only up-to 10 to 30% of the level seen in wild-type plants, suggesting that NtERF5regulated gene expression is controlling resistance to viral propagation (Fischer and Dröge-Laser 2004). OPBP1, an AP2/EREBP transcription factor, was isolated from tobacco. It has been shown that the OPBP1 can bind to an oligonucleotide containing the GCC-box

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cis element (Guo et al. 2004). Transgenic tobacco plants overexpressing the OPBP1 gene accumulated high levels of PR-1a and PR-5d genes. These transgenic plants showed enhanced resistance to the oomycete pathogen Phytopthora parasitica var. nicotianae and to the bacterial pathogen Pseudomonas syringae pv. tabaci (Guo et al. 2004). These studies suggest that ERF genes can be engineered in tobacco plants for management of viral, bacterial, and oomycete pathogens. ERF1-V, an ethylene-responsive element-factor gene of the AP2/ERF transcription factor gene family was cloned from Haynaldia villosa, a wild species of wheat. Transgenic wheat plants overexpressing EFR1-V were developed. Overexpression of the gene in wheat showed enhanced resistance to the powdery mildew pathogen Blumeria graminis f. sp. tritici (Xing et al. 2017). Overexpression of the tobacco EREBP-AP2-type transcription factor Tsi1 gene in hot pepper plants induced constitutive expression of several PR genes in the absence of stress or pathogen treatment. The transgenic hot pepper plants expressing Tsi1 exhibited resistance to Pepper mild mottle virus and Cucumber mosaic virus. These transgenic plants also showed increased resistance to the bacterial pathogen Xanthomonas campestris pv. vesicatoria and also to the oomycete pathogen Phytophthora capsici (Shin et al. 2002). Overexpression of GmERF5, a member of the soybean EAR motif –containing ERF transcription factor, showed enhanced resistance to Phytopthora sojae in soybean (Dong et al. 2015). Tomato stress-responsive factor TSRF1, an ERF protein, interacts with ethylene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum (Zhang et al. 2004; Zhou et al. 2008). Overexpression of the Medicago truncatula ERF gene, MtERF1-1, increased resistance to Rhizoctonia solani and Phytophthora medicaginis in M. truncatula, an important pasture crop (Anderson et al. 2010). Overexpression of ERF1 in Arabidopsis confers resistance to necrotrophic fungi such as Botrytis cinerea and Plectosphaerella cucumerina (Berrocal-Lobo et al. 2002). ERF1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum (Berrocal-Lobo and Molina 2004). The gene encoding HvRAF, an ERFtype transcription factor, has been isolated from young seedlings of barley. Arabidopsis thaliana plants overexpressing the barley HvRAF gene were developed. The transgenic plants showed enhanced resistance to the bacterial pathogen Ralstonia solanacearum (Jung et al. 2007). VaERF20 is an ERF gene and it was isolated from the Chinese wild Vitis genotype, Vitis amurensis. Transgenic Arabidopsis thaliana plants overexpressing VaERF20 were developed. These transgenic plants showed enhanced resistance to the fungal pathogen Botrytis cinerea and the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Wang et al. 2018). Overexpression of the Arabidopsis ERF96 gene enhanced resistance to the fungal pathogen Botrytis cinerea and the bacterial pathogen Pectobacterium carotovorum in Arabidopsis (Catinot et al. 2015; Huang et al. 2016). ERF96 enhanced the expression of the defense genes PDF1.2a, PR-3, and PR-4 by directly binding to GCC elements present in their promoters (Catinot et al. 2015). The pepper ERF transcription factor CaPF1 confers resistance to Pseudomonas syringae pv. tomato in transgenic Arabidopsis plants (Yi et al. 2004). The Arabidopsis ERF gene, AtERF15 was cloned and

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the transgenic Arabidopsis plants showed enhanced resistance against Pseudomonas syringae pv. tomato (Zhang et al. 2015), Arabidopsis AtERF014—overexpressing plants showed increased resistance to P. syringae pv. tomato (Zhang et al. 2016). Collectively these studies suggest that ERF genes are potential tools for engineering to develop disease-resistant plants.

7.4 Bioengineering EIN2 Gene to Activate Ethylene Signaling System for Crop Disease Management EIN2 is a membrane protein that acts as the central regulator of ethylene signaling pathways (Vidhyasekaran 2015; Yang et al. 2017). Accumulation of ethylene leads to activation of EIN2 (Chao et al. 1997). EIN2 is cleaved, releasing the C-terminal fragment, and moves to the nucleus and stabilizes EIN3 and EIN3-Like 1 (EIL1) (Ju et al. 2012; Qiao et al. 2012; Wen et al. 2012). EIN3 and EIL1 then regulate the expression of ERF-family transcription factors which activate plant defense responses (Solano et al. 1998). OsEIN2 was cloned from rice plants and transgenic rice plants overexpressing OsEIN2 were developed (Yang et al. 2017). The rice plants overexpressing OsEIN2 showed enhanced resistance against the rice blast pathogen Magnaporthe oryzae (Yang et al. 2017; Fig. 7.5). The results suggest that EIN2 gene is also an important tool to develop disease-resistant crop plants. 90 80 70 60

Penetration rate of pathogen (%)

50 40 30 20 10 0 Wild-type plants

Transgenic plants

Fig. 7.5 EIN2 overexpressing rice plants show enhanced resistance against Magnaporthe oryzae (Adapted from Young et al. 2017)

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7.5 Molecular Manipulation of Ethylene-Dependent Signaling System Using Microbes for Crop Disease Management 7.5.1 Rhizobacteria Pseudomonas fluorescens WCS417r is a potential rhizobacterial strain developed to activate the plant innate immunity system for management of diseases. This strain applied on roots protects leaves from bacterial, fungal and oomycete pathogens in Arabidopsis thaliana (Pieterse et al. 1998). It induced resistance against the oomycete pathogen Peronospora parasitica (Ton et al. 2002), the bacterial pathogen Pseudomonas syringae pv. tomato and the fungal pathogen Fusarium oxysporum f. sp. raphani in the model plant A. thaliana (Pieterse et al. 1996, 1998). P. fluorescens WCS417r induced ISR against Fusarium oxysporum f. sp. raphani in radish (Hoffland et al. 1995). This strain triggered ISR against Colletotrichum lindemuthianum in bean (Meziane et al. 2005) and Fusarium oxysporum f. sp. dianthi in carnation (Van Peer et al. 1991). P. fluorescens WCS417r was found to induce resistance against Fusarium oxysporum f. sp. lycopersici in tomato (Duijff et al. 1998). The rhizobacterial strain activates the plant innate immune system, triggering several defense mechanisms. It induced the formation of structural barriers, such as papillae due to the deposition of callose and the accumulation of phenolic compounds in the cell walls at the site of pathogen attack (Benhamou et al. 1996, 1998; M’Piga et al. 1997). Application of P. fluorescens WCS417r induces thickening of cell walls in tomato (Duijff et al. 1997). Knoester et al. (1999) showed that ethylene signaling system is involved in P. fluorescens WCS417r—triggered ISR in A. thaliana. The Arabidopsis mutant eir1 is insensitive to ethylene in the roots, but not in the shoots. When the WCS417r strain was applied to the roots, it could not trigger ISR. By contrast, the rhizobacterial strain induced ISR when it was infiltrated into the leaves (Knoester et al. 1999). The results suggest that ethylene responsiveness is required at the site of application of the rhizobacterial strain for induction of ISR in Arabidopsis. The Arabidopsis eds mutants showed reduced sensitivity to ethylene and these mutants were non-responsive to expression of ISR upon root colonization by the rhizobacterial strain P. fluorescens WCS417r (Ton et al. 2002). The rhizobacterial strain WCS417r was not capable of inducing resistance against P. syringae pv. tomato in the ethylene-insensitive Arabidopsis mutant etr1 (Pieterse et al. 1998) These studies suggest that ethylene signaling is important component in WCS417r-activated innate immune system in Arabidopsis. A R2R3-MYB-like transcription factor, MYB72, has been shown to be involved in triggering defense responses against broad-spectrum of pathogens in Arabidopsis thaliana (Van der Ent et al. 2008). P. fluorescens WCS417r induces systemic resistance (ISR) in A. thaliana. The transcription factor MYB72 gene was specifically activated in the A. thaliana roots upon colonization by P. fluorescens WCS417r. T-DNA knockout mutants myb72 were incapable of mounting ISR against the pathogens,

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indicating that MYB72 is involved in activating the defense responses. However, overexpression of MYB72 did not result in enhanced resistance against the pathogens, suggesting that MYB72 is not sufficient for the expression of ISR. MYB72 interacts with the Ethylene Insensitive-Like3 (EIL3) transcription factor. P. fluorescens WCS417r may trigger enhanced expression of MYB72 and the activated MYB72 gene may interact with EIL3 transcription factor, resulting in activation of ET signaling system (Van der Ent et al. 2008). EIL proteins act as the key transcription factors of ET-regulated gene expression and act as positive regulators of ET signaling (Guo and Ecker 2004). They bind to promoters of ET-responsive genes, such as ERF1 and initiate a transcriptional cascade leading to the expression of ET-targeted genes (Solano et al. 1998). Collectively these results suggest that MYB72, EIL3 and ERF1 are part of signaling network involved in the plant’s defense response induced by P.fluorescens WCS417r. Another P. fluorescens strain, P. fluorescens WCS374r, triggers resistance against the bacterial pathogen P. syringae pv. tomato through activation of ET signaling system (Ran et al. 2005b). The rhizobacterium was isolated from the rhizosphere of potato. It suppresses Fusarium wilt of radish caused by Fusarium oxysporum f. sp. raphani (Leeman et al. 1995a, b). Seed treatment with the strain coated with 1% methyl cellulose reduced the Fusarium wilt incidence by about 42% and increased the yield by about 45% when compared with untreated control in radish crop (Hoffland et al. 1995; Leeman et al. 1995b). It has also been found useful in management of the bacterial wilt disease caused by Ralstonia solanacearum in Eucalyptus urophylla (Ran et al. 2005a). Application of P. fluorescens WCS374r to soil induced resistance in rice leaves against the blast pathogen Magnaporthe grisea. Plants colonized by the WCS374r strain showed a 47% reduction in lesion number (De Vleesschauwer et al. 2008). P. fluorescens WCS374r strain elicits ISR against the rice blast fungal pathogen M. oryzae through JA/ET-regulated pathway (De Vleesschauwer et al. 2008). P. fluorescens WCS374r triggers resistance against the bacterial pathogen P. syringae pv. tomato through ET signaling system (Ran et al. 2005b). It has also been found useful in management of the bacterial wilt disease caused by Ralstonia solanacearum in Eucalyptus urophylla (Ran et al. 2005a). Pseudomonas chlororaphis 06 is another rhizobacterium which induces defense response through activation of ET signaling system. It induces resistance against the soft rot bacterial pathogen Erwinia carotovora subsp. carotovora in tobacco. The tobacco plants were transformed with a mutant etr1 gene to reduce ethylene sensitivity in these plants. These transformed plants did not display induced resistance to E. carotovora when colonized by P. chlororaphis 06 strain, suggesting that the rhizobacterial strain triggers the plant immune system through the ET signaling system (Spencer et al. 2003). Bacillus subtilis strain GBO3 triggered ISR in Arabidopsis through an ethylenedependent pathway, albeit independent of the SA or JA signaling pathways (Ryu et al. 2004). B. subtilis GB03 strain has been developed as a commercial product which is designated as Kodiak by Gustafson (Brannen and Kenney 1997) and as Companion by Growth Products (Haas and Défago 2005). It is effective in controlling Fusarium and Rhizoctonia pathogens in cotton crop (Brannen and Kenney 1997). Seed treatment

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with B. subtilis GB03 resulted in reductions in severity of the angular leaf spot of cucumber caused by Pseudomonas syringae pv. lachrymans (Raupach and Kloepper 2000).

7.5.2 Trichoderma Trichoderma spp. are potential biocontrol agents to manage several soil-borne pathogens (Vidhyasekaran 2004, 2007a). Trichoderma asperellum (T. harzianum) triggers induced systemic resistance (ISR) against several pathogens (Yedidia et al. 1999, 2000, 2003; Harman et al. 2004; Shoresh et al. 2005). Ethylene signal transduction pathway has been shown to be involved in the ISR induced by T. asperellum (Shoresh et al. 2005). Application of an inhibitor of ethylene action (silver thiosulfate, STS) strongly inhibited or completely abolished the protective effect of T. asperellum on plants (Shoresh et al. 2005), suggesting the involvement of ethylene signaling system in T. asperellum triggered disease resistance. T. asperellum does not trigger ethylene biosynthesis in cucumber plants. No significant difference in production of ethylene was observed between Trichodermaapplied and control (without Trichoderma application) plants (Shoresh et al. 2005). However expression levels of the two genes, ETR1 and CTR1, in the ethylene signaling pathway were very much affected in Trichoderma-applied plants (Shoresh et al. 2005). ETR1 is a receptor of ethylene. Ethylene signal transduction is initiated by the binding of ethylene to the receptor (Binder et al. 2012; Shakeel et al. 2013). The receptor is localized to endoplasmic reticulum (Grefen et al. 2008). The receptor has transmemrane domain near its N-terminus and putative signaling motifs in the C-terminal half. The predicted transmembrane domain at the N-terminus comprises the ethylene-binding domain (EBD) (Grefen et al. 2008). The receptor N-terminus has three to four transmembrane domains that bind ethylene (Shakeel et al. 2013). CTR1 is a Raf-like Ser/Thr kinsase. It functions as a key mediator of ethylene signal transduction, acting just downstream of ETR1. It negatively regulates ethylene signaling (Yoo et al. 2008; Vidhyasekaran 2015). The receptor ETR1 also negatively regulates ethylene signaling (Qu and Schaller 2004; Gao and Schaller 2009). ETR1 physically interacts with CTR1 (Gao et al. 2003) and its major function in ethylene signaling is the maintenance of CTR1 in an active state (Qu et al. 2007). The major action of Trichoderma appears to be suppression of the action of both ETR1 and CTR1, the negative regulators of ethylene signaling. By suppressing the negative regulators, Trichoderma activates ethylene signaling resulting in increased expression of plant defense genes (Shoresh et al. 2005).

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7.5.3 Pythium oligandrum Pythium oligandrum is a biocontrol agent which controls several soil-borne fungal and bacterial pathogens (Benhamou et al. 1997; Picard et al. 2000; Takenaka et al. 2003; Hase et al. 2006). When tomato plants were treated with the mycelial homogenate of P. oligandrum, the plants showed reduced incidence of the bacterial wilt caused by Ralstonia solanacearum (Hase et al. 2006). The elicitor from P. oligandrum triggered ethylene signaling pathway in tomato (Takahashi et al. 2006). ACC (1-aminocyclopropane-1-carboxylic acid) oxidase is a key enzyme in biosynthesis of ethylene. It catalyzes ACC to ethylene (Vidhyasekaran 2007b, 2015). ACC oxidase was up-regulated more than tenfold by the elicitor in tomato roots (Takahashi et al. 2006). It strongly suggests that P. oligandrum may activate ethylene signaling system and induce host plant defense response (Hase et al. 2006). P. oligandrum treatment induced biosynthesis of ethylene. The increase in ethylene content was about 11-fold higher in the P. oligandrum-treated plants compared to distilled water-treated control plants (Fig. 7.6; Hase et al. 2006). P. oligandrum also activated ethylene signaling pathway. Activation of the ethylene-dependent signaling pathway was accompanied by increased expression of genes encoding ethylene receptors and ethylene-responsive transcription factors. Transcripts of ethylene receptor LeETR4 and ethylene-inducible transcription factor LeERF2 genes were found to be induced in the roots of P. oligandrum–treated tomato roots (Hase et al. 2006). Activation of ethylene-dependent signaling pathway resulted in enhanced expression of three pathogenesis-related protein genes. PR2b, PR-3b, and PR-5b genes were found to be induced in tomato roots treated with P. oligandrum. The induced expression of ethylene signaling pathway resulted in reduction of bacterial wilt disease caused by R. solanacearum in tomato (Hase et al. 2006). These results suggest that P. oligandrum is a powerful tool to trigger ethylene signaling system for management of crop diseases.

Fig. 7.6 Pythium oligandrum induces enhanced ethylene biosynthesis in tomato plants (Adapted from Hase et al. 2006)

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